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First published online July 20, 2007
Journal of Experimental Biology 210, 2706-2713 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.000703
Mucus function and crossflow filtration in a fish with gill rakers removed versus intact
Department of Biology, College of William and Mary, PO Box 8795, Williamsburg, VA 23187-8795, USA
Author for correspondence (e-mail:
slsand{at}wm.edu)
Accepted 20 March 2007
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Summary |
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Key words: suspension feeding, filter feeding, hydrosol filtration, tilapia, Oreochromis aureus
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). These fish belong to 21 families in 12 orders
(Cheer et al., 2001), and
comprise a quarter of the world fish catch
(Food and Agriculture Organization of the
United Nations, 2000). Despite the ecological and economic
importance of suspension-feeding fish, food particle retention mechanisms are
known for only seven species, including two species of tilapia
(Callan and Sanderson, 2003;
Hoogenboezem et al., 1991;
Sanderson et al., 2001).
Endoscopic analysis of the oropharyngeal cavity during suspension feeding
in the Nile tilapia (Oreochromis niloticus Linnaeus, Cichlidae)
described hydrosol filtration with entrapment of particles in mucus on the
gill rakers and branchial arches as one mechanism of particle encounter and
retention (Sanderson et al.,
1996). During hydrosol filtration, particles that are suspended in
water contact filter elements as a result of physical processes [i.e. direct
interception, inertial impaction, gravitational deposition, diffusional
deposition, and electrostatic attraction
(LaBarbera, 1984;
Rubenstein and Koehl, 1977;
Shimeta and Jumars, 1991)]. If
the filter elements are sticky due to the presence of mucus, a particle that
encounters a filter element during hydrosol filtration can be retained by
adhesion, even if the particle is small enough to pass between the filter
elements. In O. niloticus, mucus containing the trapped particles is
then transported to the esophagus for swallowing
(Sanderson et al., 1996).
In contrast, a second species of tilapia, O. esculentus (Graham),
lacks observable mucus in the oropharyngeal cavity and uses crossflow
filtration instead of mucus to retain particles during suspension feeding
(Goodrich et al., 2000;
Sanderson et al., 2001).
During crossflow filtration, hydrodynamic forces such as inertial lift cause
particles to remain suspended but become concentrated in the fluid traveling
parallel to the filter surface, as filtrate exits between the filter elements
(Brainerd, 2001;
Sanderson et al., 2001). Thus,
the fluid in the oropharyngeal cavity becomes increasingly more concentrated
with food particles as the suspension is reduced in volume while traveling
towards the esophagus. The particles are then swallowed with very little
accompanying water (Sanderson et al.,
2001).
Oreochromis esculentus is typically described as a specialist,
feeding mostly on phytoplankton or colonial blue-green algae
(Onyari, 1983). The dietary
breadth of O. niloticus is much wider, consisting of phytoplankton,
filamentous algae and diatom-rich sediments as well as insect larvae, benthos
and crustaceans (Onyari,
1983). To investigate whether there is a correlation between diet
and particle retention mechanism in suspension-feeding tilapia, we used a
fiberoptic endoscope to study intra-oral movements of particles during feeding
in O. aureus (Steindachner), a species with a similar ecological
niche to O. niloticus (Drenner et
al., 1984; Mallin,
1985; Spataru and Zorn,
1978). As so few data are available on particle retention
mechanisms in suspension-feeding fish, such a correlation could be a powerful
predictive tool for gaining insight into the ecological implications and
evolution of suspension-feeding mechanisms. Based on the dietary similarities
between O. aureus and O. niloticus, we predicted that O.
aureus uses mucus to retain particles on the branchial arches.
Gill rakers attached to the branchial arches have been hypothesized to be a
component of all filtration mechanisms in fish
(Hoogenboezem et al., 1991;
Sanderson et al., 1991;
Sanderson et al., 1996;
Sanderson et al., 2001). In
tilapia, toothed projections (
150 µm high) on the external faces of
the arches, termed microbranchiospines, have also been proposed as filtering
structures (Beveridge et al.,
1988a; Beveridge et al.,
1988b). However, surgical removal of all rakers and
microbranchiospines from the suspension-feeding tilapia Sarotherodon
galilaeus did not significantly affect the size distribution of ingested
particles or the efficiency of particle retention
(Drenner et al., 1987).
Sanderson et al. (Sanderson et al.,
1996) suggested that Drenner et al.'s results could be explained
if mucus on the arches functions to retain particles during hydrosol
filtration after the rakers have been removed.
We used a fiberoptic endoscope to quantify and compare the intra-oral movements of particles in the presence versus the absence of rakers and microbranchiospines in O. aureus. The effects of raker removal on mucus presence and particle movement inside the oral cavity have not been studied in any fish species. We removed the rakers and microbranchiospines from all branchial arches. Our objective was to test the hypothesis that mucus, if present on the branchial arches, functions to retain particles during hydrosol filtration before and after removal of the gill rakers in O. aureus.
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Materials and methods |
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). Five
specimens (20.3–23.4 cm standard length, SL) were used for the
endoscopy experiments. Fish were anesthetized with MS-222 and a polyethylene
cannula (45 cm long, 2.15 mm i.d., 3.25 mm o.d., Intramedic PE 280, Sparks,
MD, USA) was implanted into the oropharyngeal cavity through a hole drilled in
the left preopercular bone. To prevent the cannula from being pulled through
the hole, a flange (approximately 1 mm wide) around the circumference of one
end of the cannula lay flush with the tissue of the oropharyngeal cavity. The
cannula fitted snugly, eliminating any water flow through the hole in the
preopercular bone. The external section of the cannula was then threaded
through a second flanged polyethylene cannula (2.5 cm long, 3.76 mm i.d., 4.82
mm o.d., Intramedic PE 360), preventing any slippage back into the
oropharyngeal cavity. To reduce irritation, a small piece of neoprene rubber
(0.8 cmx0.8 cm) was placed between the second flanged cannula and the
skin. After this the fish was returned to the aquarium. The experiments were conducted 4 h after cannula implantation. A flexible fiberoptic endoscope (ultrathin fiberoptic type 14, 1.4 mm o.d., 1.2 m working length, 75° field of view, 0.2–5.0 cm depth of field, Olympus, New York, NY, USA) was threaded through the cannula. The endoscope was attached to an Intensified Imager VSG (50–500 Hz, Kodak, San Diego, CA, USA). An Ektapro Hi-Spec Motion Analyzer 1012/2 (Kodak, San Diego, CA, USA) with split-screen imaging was used to record external views of the oral jaws simultaneously with the endoscopic views, to correlate external feeding behaviors with the movements of intra-oral structures and particles in the internal endoscopy video. A high-intensity light source (Helioid ALS-6250, 250 W, Olympus) provided light for the endoscope. A Sony DSR-11 DVCAM video recorder with a jog shuttle (remote control unit DSRM-20, Sony, Tokyo, Japan) was used for frame-by-frame analysis of the videotapes. The digitized video images used for publication were processed by convolving them with a mean kernel (4x4 pixels) using NIH Image 1.62, which smoothed the fine honeycomb pattern caused by individual fibers in the fiberoptic bundle.
Data were recorded as fish were fed a slurry of finely crushed TetraminTM flakes (0.1–1.0 mm diameter) mixed with water. Pre-hydrated brine shrimp cysts (Artemia sp., 210–300 µm) were added to the slurry to serve as additional tracer particles when viewed through the endoscope. The slurry was administered into the water directly above the fish through a short tube attached to a 30 ml syringe. Tilapia engulfed particles directly from the tip of the tube or as the particles descended through the water column. Fish were anesthetized for cannula removal at the conclusion of each experiment, following which the insertion site healed fully.
Gill raker removal
The method of raker removal was modified from that of Drenner et al.
(Drenner et al., 1987). O.
aureus were anesthetized with MS-222 and the tissue supporting all
lateral and medial rakers and microbranchiospines was removed with
microforceps from the anterior four branchial arches on both sides of five
fish. The fifth arches form the lower pharyngeal jaw, which was left
unaltered. The procedure lasted an average of 90 min, during which the fish
was lifted periodically from the water containing MS-222 to remove a section
of rakers and microbranchiospines, and then returned to the water in the
surgery tray. The fish was then returned to its aquarium and Fungus Eliminator
(5 g 20 l–1; Jungle Laboratories Corporation, Cibolo, TX,
USA) was added once to prevent infection. Fish were not adversely affected by
the surgery and exhibited normal feeding behavior within 2 days. During the 15
days following surgery, the arches healed as described by Drenner et al. for
Sarotherodon galilaeus (Drenner
et al., 1987). Endoscopy experiments were conducted on fish with
rakers intact and again on the same individuals 15 days after raker
removal.
Mucus presence and classification
For each of five specimens, endoscopic video footage of slurry feeding and
ventilation were analyzed frame-by-frame for the presence of mucus before and
after removal of rakers and microbranchiospines. First, the sequences with the
clearest, most focused views were identified. From these, 2–4 sequences
per fish were chosen at random for analysis. All video frames containing mucus
were then analyzed and categorized as follows. (1) The number of sequences and
the number of video frames in which each of the following types of mucus was
observed: (a) aggregate (an irregularly shaped opaque clump), (b) strand (a
single opaque string of mucus), (c) sheet, stretching across the entire field
of view while covering the rakers or passing through the field of view. (2)
The movement of mucus: (a) pass (mucus moved through the field of view without
contacting any oropharyngeal surface), (b) lift and pass (mucus that had been
attached to the arches and rakers visibly lifted and exited from the field of
view), (c) sliding along arches (mucus maintained contact with the arches
and/or rakers while traveling posteriorly), (d) attached (mucus maintained
contact with the arches and/or rakers and did not change location). (3) The
action of the fish as mucus that had been attached to the arches and rakers
lifted and exited from the field of view: (a) pumps, (b) reversals or (c)
ventilation. Data are reported as means ± s.d. unless stated
otherwise.
Particle analysis
Frame-by-frame video analysis of 100 slurry particles or brine shrimp cysts
passing the endoscopic field of view during feeding was conducted for each of
three specimens with rakers intact, as well as after raker removal. For this
analysis, 25–50 particles (33±12, N=18 sequences) were
selected randomly within each of 2–4 feeding sequences per specimen. The
movement of each particle was described as one of four actions: (1) straight,
passed the field of view in a posterior direction without contacting any
oropharyngeal surface; (2) bounced, particle was seen to graze or bounce off
either the oral roof, the branchial arches, or a raker before continuing
posteriorly; (3) disappeared, particle traveled towards the arches and
disappeared either between two rakers or between two of the arches; (4) stuck,
particle stayed immobile on the arches or rakers before traveling
posteriorly.
To determine the extent to which mucus was involved in particle capture, the longest feeding sequence with the best lighting in which mucus was present was analyzed for two fish with rakers intact. All slurry particles and brine shrimp cysts passing through the field of view (volume of approximately 1 ml) during this feeding sequence were counted. The number of particles caught in mucus during the course of the feeding sequence was then tallied and compared to the total number of particles passing through the field of view during the sequence.
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Pumps and reversals
O. aureus suspension-fed on the TetraminTM slurry using a
series of pumping actions. During a feeding pump, water entered the mouth and
continued to flow posteriorly through the oropharyngeal cavity (see Movie 1 in
supplementary material) until exiting via the operculum. Pumps were
frequently interrupted by a reversal, during which all of the suspended
particles were seen through the endoscope to travel with the water from
posterior to anterior inside the oropharyngeal cavity. This reversal of flow
to a posterior to anterior direction has been termed stage 1 of a reversal
(Sanderson et al., 1996).
During stage 2 of a reversal, the particles were viewed resuming an anterior
to posterior flow inside the oropharyngeal cavity.
Mucus presence and classification with gill rakers intact
A frame-by-frame video analysis of five O. aureus during
suspension feeding on slurry and during ventilation was conducted on a total
of 29 641 and 28 749 frames, respectively, (125 Hz) before raker removal.
During feeding, mucus was present in 53±37% of the frames analyzed,
compared to mucus present in 61±26% of the video frames analyzed during
ventilation.
Mucus was identified as belonging to one of six categories when viewed through the endoscope: strand, aggregate, sheet, both strand and sheet viewed simultaneously, both aggregate and sheet viewed simultaneously, or both strand and aggregate viewed simultaneously (Table 1). Only one category of mucus was present within each video frame. However, since more than one category of mucus was observed consecutively within some feeding or breathing sequences, the percentage of sequences during which each category was observed totals to more than 100% in Table 1. Whether quantifying frequency of occurrence for each mucus category using percentage of sequences or percentage of video frames during which mucus in that category was observed, mucus appeared as opaque sheets most frequently. These mucus sheets could often be seen to extend across the entire endoscopic field of view.
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In general, mucus remained attached to the arches and swayed (57±28% of frames with mucus during feeding, 98±3% of frames with mucus during ventilation). Less frequently, the mucus lifted from the arches and traveled posteriorly (28±26% of frames analyzed during feeding, 0% of frames analyzed during ventilation; see Movie 2 in supplementary material). Mucus sometimes passed through the endoscopic field of view during feeding (15±20%) and ventilation (2±3%) without contacting any oropharyngeal surface. Mucus was never observed sliding across the arches.
Mucus that was attached to the arches often remained on the arches for a long period of time before exiting from the field of view. To quantify the duration of mucus presence in four fish, a total of ten sequences with a mucus strand or aggregate were observed until the mucus exited from the field of view or until the endoscopic sequence ended. Mucus remained attached for a large number of pumps and reversals before the mucus lifted from the arches or the endoscopy sequence ended (Table 2). The data on duration of attached mucus for O. aureus in Table 2 are conservative, since the mucus was still attached when some sequences ended.
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Stage 2 of a reversal following a pump was the most common action during which mucus that had been attached to the arches subsequently left the field of view in a posterior direction after being lifted off the arches during stage 1 of a reversal (65% of 23 total occurrences of mucus during feeding for five fish) (Fig. 1; see Movie 3 in supplementary material). The exit of previously attached mucus from the field of view in association with a pump was less common (35% of total occurrences for five fish). Attached mucus was never dislodged and carried posteriorly during ventilation.
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For five O. aureus combined, TetraminTM flake particles or brine shrimp cysts were seen trapped in mucus during 15% of the 12 744 frames (125 Hz) with mucus present that were analyzed during feeding. To ascertain the effectiveness of mucus in particle retention, a typical feeding sequence was analyzed for each of two fish to determine the total number of particles that passed through the endoscopic field of view compared with the total number of particles that were retained in mucus during the feeding sequence. Of the total of 642 particles that passed posteriorly during the two feeding sequences, 98% traveled independently without being retained in the mucus while only 2% of the particles were retained in mucus on the arches or rakers.
Mucus and particle analysis with gill rakers removed
Typical feeding behavior was observed after the rakers were removed. There
were no observable differences in the number of sequential pumps or the
frequency of reversals during suspension feeding in the absence of rakers.
Just as when the rakers were intact, no food particles were visible exiting
via the operculum after the rakers had been removed.
Frame-by-frame analysis of post-raker removal endoscopic videotapes from three specimens included all unobstructed, clearly focused views (52 063 frames of feeding on slurry and 8020 frames of ventilation, 125 Hz). No mucus was seen during ventilation without rakers, and the total number of frames with mucus present during suspension feeding (2±2%) was greatly reduced compared to endoscopy with intact rakers. During the limited number of suspension-feeding frames with mucus after the removal of rakers, there was an equal percentage (33% of frames with mucus present) of strands, aggregates and sheets of mucus visible through the endoscope. Mucus swayed while attached to the arches until lifted from the arches (stage 1) and cleared from the field of view (stage 2) with a reversal in 51% of the frames in which mucus was present during feeding. Mucus was also frequently seen passing straight through the field of view in a posterior direction without contacting any oropharyngeal surface during feeding pumps (49% of total frames analyzed).
For each of the three fish, 100 brine shrimp cysts or slurry particles were followed through the field of view to determine particle movement while suspension feeding after raker removal. The majority of the particles (84±21%, Table 3) traveled posteriorly in a straight path without touching any oropharyngeal surface. Many particles were visible through the endoscope while traveling straight towards the arches, and then disappeared into the dark void between two arches (15±21%).
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) hypothesized that cichlid suspension feeders that retain
bacteria and phytoplankton use hydrosol filtration with mucus entrapment, as
does O. niloticus. A hydrosol filter can extract a wide range of
particle sizes, including particles smaller than the pore size between the
filter elements, because particles can be retained on sticky surfaces of a
hydrosol filter. Since particles can be retained as water passes over instead
of through the filter, a hydrosol filter is less prone to clogging than a
sieve on which particles larger than the pores of the mesh are retained when
filtrate exits through the pores. Perhaps the most notable advantage of using
hydrosol filtration with mucus entrapment is that the particles are bound in
mucus ready for transport to the esophagus
(Sanderson et al., 1991;
Sanderson et al., 1996).
Based on the similarities in diet and ecological niche of O.
niloticus and O. aureus, we hypothesized that O. aureus
uses hydrosol filtration with mucus entrapment. Although O. aureus
with rakers intact had mucus present twice as often during feeding as O.
niloticus (53% of the video frames analyzed versus 26%,
respectively), the mucus did not appear to serve as a particle entrapment
mechanism in O. aureus. Particles were seen trapped in mucus 97.9% of
the time when mucus was present during feeding in O. niloticus
(Sanderson et al., 1996), but
only 15% of the time in O. aureus. The percent of particles trapped
in mucus during feeding on TetraminTM slurry was higher in O.
niloticus (54%) compared to O. aureus (2%). Overall, brine
shrimp cysts (210–300 µm diameter) and slurry particles
(0.1–1.0 mm diameter) were retained much less frequently in O.
aureus mucus than in O. niloticus mucus. Our data on O.
aureus demonstrate that the presence of mucus strands, sheets and
aggregates inside the oral cavity during suspension feeding is not necessarily
indicative of the use of mucus to trap particles. The infrequent occurrence of
particles retained in mucus in O. aureus compared to O.
niloticus does not support the prediction
(Sanderson et al., 1996) that
cichlid suspension feeders that retain phytoplankton and cyanobacteria will
use mucus entrapment.
As observed in O. esculentus
(Goodrich et al., 2000), the
majority of particles (98%) in O. aureus traveled posteriorly without
contacting mucus or the arches. These results demonstrate that O.
aureus, like O. esculentus, uses crossflow filtration as a
particle retention mechanism (Sanderson et
al., 2001). During crossflow filtration in pump suspension-feeding
fish, water is pumped parallel to the rakers, transporting particles towards
the esophagus. As the oral cavity narrows posteriorly, particles remain
suspended in the mainstream flow above the rakers and become more concentrated
as filtrate exits between the rakers
(Brainerd, 2001;
Sanderson et al., 2001).
The filtration mechanisms of the three tilapia species that have been
studied with a fiberoptic endoscope can be placed along a continuum from
O. niloticus, with its combination of crossflow filtration and mucus
entrapment (Sanderson et al.,
1996), to O. aureus, with crossflow filtration in the
presence of mucus, but not mucus entrapment, to O. esculentus, with
crossflow filtration in the absence of mucus
(Goodrich et al., 2000;
Sanderson et al., 2001).
Dead-end sieving by rakers and/or microbranchiospines, during which the fluid
to be filtered passes perpendicularly through the pores between the rakers
and/or the microbranchiospines while particles larger than the pores are
retained on the sieve, is not used as a filtration method in any of these
three species (Sanderson et al.,
1996; Sanderson et al.,
2001). While muscular control of rakers during feeding has been
hypothesized to allow reduction in the diameter of the channels between rakers
in common bream (Hoogenboezem et al.,
1991; van den Berg et al.,
1994), changes in channel diameter as a result of raker movement
have not been observed to occur in endoscopic videotapes of tilapia species
(Goodrich et al., 2000;
Sanderson et al., 1996;
Sanderson et al., 2001).
Correlation between diet and particle retention mechanism
Diet analysis of O. niloticus and O. aureus showed
similarities in the prey species ingested in the field. However, there is some
evidence from the literature suggesting that O. niloticus has a
greater ability to retain small particles than does O. aureus,
supporting the hypothesized link
(Sanderson et al., 1996)
between mucus entrapment and the retention of small food particles.
Cyanobacteria such as Anabaena and Microcystis (cell
dimensions as small as 2 µmx3 µm) are common elements in the diet
of both species (Moriarty and Moriarty,
1973; Northcott et al.,
1991; Spataru and Zorn,
1978). However, ingestion rates calculated for O. aureus
feeding on Anabaena appear to be less than that of O.
niloticus, although this could be due to starvation of O.
niloticus prior to experimentation
(Northcott et al., 1991).
O. aureus lost mass when presented with Chlamydomonas (6
µm–15 µm), which suggests an inability to filter smaller particles
efficiently (McDonald, 1987).
Sanderson et al. (Sanderson et al.,
1996) showed that O. niloticus relies more on mucus to
retain small particles (TetraminTM slurry particles, 0.1–1.0 mm in
diameter) than larger particles (whole TetraminTM flakes, 3–10 mm
diameter).
Unlike O. niloticus, O. esculentus appears to be unable to retain
2-celled colonies of Scenedesmus
(Batjakas et al., 1997). In
addition, O. niloticus consumed significantly more 3- to 4-celled
Scenedesmus colonies (c. 30 µm longx18 µm diameter)
(Goodrich et al., 2000) than
O. esculentus (Batjakas et al.,
1997). Thus, the abilities of O. niloticus, O. aureus and
O. esculentus to extract small particles differ, with O.
niloticus able to retain the smallest particles.
The dietary data discussed above and data from endoscopic videotapes support the hypothesis that the entrapment of particles in mucus during hydrosol filtration in O. niloticus allows for the retention of smaller particles than does crossflow filtration in O. esculentus and O. aureus. Our study demonstrated that mucus that is visible in the oropharyngeal cavity during suspension feeding in O. aureus is not used to retain particles during hydrosol filtration. While the available data indicate a correlation between the smallest particle size in the diet and the particle retention mechanism used by each of these three species, we did not find a correlation between range of particle size in the diet and particle retention mechanism in these tilapia species. O. niloticus and O. aureus both have a more generalized diet with a greater range of food particle sizes than O. esculentus, but the particle retention mechanism in O. niloticus differs from that of O. aureus and O. esculentus.
Role of mucus
All mucus attached to the arches was observed for O. niloticus
(Sanderson et al., 1996) and
O. aureus, until either the mucus was lifted off the arches or the
endoscopy sequence ended. Mucus remained attached during fewer pumps and
reversals before lifting off the arches in O. niloticus than in
O. aureus. During feeding in three O. niloticus, 60 mucus
strands and aggregates remained attached to the arches during a total of only
21 pumps and six reversals before lifting off or sliding along the arches
(Sanderson et al., 1996).
However, during feeding in four O. aureus, ten mucus strands,
aggregates, and/or sheets remained attached to the arches during 41 pumps and
22 reversals without lifting off or sliding along the arches
(Table 2). Another distinction
between the two species is that opaque sheets of mucus extending across the
arches were not present in O. niloticus
(Sanderson et al., 1996), but
were the most common category of mucus observed in O. aureus
(Table 1).
Thus, mucus is present more often during feeding in O. aureus than
in O. niloticus, and the mucus remains attached to the arches during
more pumps and reversals in O. aureus before being lifted and
transported to the esophagus, but particles are being trapped in mucus less
frequently in O. aureus. There are no indications that this
difference in mucus function between the two species can be accounted for by
differences in oral flow patterns or flow speed (J.C.S. and S.L.S.,
unpublished). A possible explanation that deserves study is that the mucus may
have different properties in these two species. The glycoproteins present in
fish mucus can either remain neutral or, in the presence of sialic acid or
sulphated monosaccharides, become acidic. The full extent to which the
glycoproteins influence the properties or contribute to specific functions of
mucus is still controversial (Shephard,
1994). Based on the similar composition of fish and mammalian
mucus, Northcott and Beveridge (Northcott
and Beveridge, 1988) hypothesized that the viscosity of fish mucus
may increase as acidic glycoprotein content increases.
A histological study of the gill rakers and branchial arches in O.
niloticus revealed two morphologically distinct types of mucus cells
(Northcott and Beveridge,
1988). The mucus cells located on the trailing keel of the rakers
were large, clavate cells that produced an acidic mucosubstance. Northcott and
Beveridge (Northcott and Beveridge,
1988) suggested that this mucus with charged acidic groups may
have increased particle retention properties. Smaller goblet cells lined the
anterior face and side of the arches and secreted neutral or neutral/acidic
mucus. This mucus may be less viscous and could aid in transport of captured
particles towards the esophagus (Northcott
and Beveridge, 1988). Differences in types of mucus produced are
evident not only in different areas of the oropharyngeal cavity, but also
among different species. From a histological study of the gills and epidermis
of plaice, flounder and trout, Fletcher et al. suggested that the type of
mucus produced by goblet cells in the arches and epidermis of fish could vary
depending on the habitat of each species
(Fletcher et al., 1976). In
Oreochromis mossambicus, the proportions of mucosubstances present in
the oral mucosa even varied seasonally. During mouthbrooding, the
concentrations of glycogen, sialomucins and sulfomucins increased compared to
non-brooding seasons (Varute and Jirge,
1971). Thus, the oropharyngeal mucus of O. aureus may
differ in acidity and viscosity from that of O. niloticus, and
consequently differ in function.
Since the mucus is not serving as the primary particle entrapment mechanism
in O. aureus, are there potential functions for the abundant mucus
that is present? Mucus can form unstirred layers over surfaces that are
involved in ion or water transport
(Shephard, 1994). An unstirred
layer is a static region of fluid immediately adjacent to a membrane that does
not mix even when the bulk solution is stirred. Thermal convection or density
gradients do not cause significant mixing of the region of slow laminar flow
over the static layer (Barry and Diamond,
1984).
Possible water- and ion-regulatory roles for mucus are based on the
formation of these unstirred layers
(Shephard, 1994). We propose
that a potential function for mucus in crossflow filtration is to contribute
to the formation of an unstirred layer and thereby enhance the use of the
branchial arches as a surface that leads to the radial migration of particles.
Lift is a hydrodynamic force that causes particles flowing in suspension
inside tubes or channels to migrate radially towards the center of the tube at
a tube Reynolds number (Re)>1. The oral cavity Re for
O. aureus, calculated using the dorso-ventral height of the oral
cavity and the mean peak flow speed during feeding pumps, was 300. At
Re>1, particles lift away from the tube walls and migrate radially
as they travel downstream (Eloot et al.,
2004; Matas et al.,
2004). This radial migration is an important component of
crossflow filtration because particles that remain suspended in the crossflow
are not lost through the pores of the filter, nor do the suspended particles
clog the pores. The formation of an unstirred layer directly over each arch
and between the rakers could reduce the effective sizes of the pores between
the rakers and between the arches of the branchial filter. Inertial lift
increases as the square of the crossflow velocity
(Chellam and Weisner, 1992). By
helping to regulate the loss of water between the rakers and between the
arches, mucus could increase the crossflow speed inside the oropharyngeal
cavity and thereby increase inertial lift.
Whereas hydrosol filtration mechanisms are either independent of particle
radius or dependent on particle radius to the first power
(Rubenstein and Koehl, 1977;
Shimeta and Jumars, 1991),
inertial lift increases as the cube of the particle radius
(Chellam and Weisner, 1992).
Thus, crossflow filtration using inertial lift is predicted to exhibit greater
dependence on particle size than is hydrosol filtration using mucus
entrapment. The inability of O. esculentus and O. aureus to
retain particles as small as those retained by O. niloticus
(Batjakas et al., 1997) (J.C.S.
and S.L.S., unpublished) is consistent with the reliance of these two species
on inertial lift generated during crossflow filtration rather than the use of
hydrosol filtration.
One notable difference in mucus transport between O. niloticus and
O. aureus was the absence of mucus sliding across the arches in
O. aureus. O. niloticus uses feeding pumps for sliding transport of
mucus and retained particles towards the esophagus. Whereas mucus was observed
sliding along the arch surfaces before being transported out of the field of
view in 29% of 59 total mucus occurrences during feeding in O.
niloticus (Sanderson et al.,
1996), mucus was never observed sliding across the arches in
O. aureus. The lack of sliding for mucus transport in O.
aureus is consistent with mucus remaining attached to the arches for a
longer duration before being lifted prior to transport posteriorly. The lack
of sliding is also consistent with the use of mucus, particularly the frequent
sheets and aggregates (Table
1), as a mechanism in O. aureus to restrict the
inter-raker gap distance rather than as a hydrosol filtration mechanism.
Mucus and particle analyses before versus after gill raker removal
The large decrease in mucus presence after raker removal in O.
aureus (53% of frames during feeding versus 2% of frames during
feeding) can be explained in part by the location of tilapia mucus cells at
the base of the rakers, primarily along the arch between the medial and
lateral rows of rakers (Northcott and
Beveridge, 1988). Surgical removal of gill rakers in O.
aureus did not significantly affect the movement of particles inside the
oropharyngeal cavity. Regardless of whether the rakers were intact or removed,
84% of particles traveled posteriorly without contacting any oropharyngeal
surface (Table 3). In the
absence of rakers, slightly more particles were observed disappearing between
the arches (15%) than with rakers intact (8%), but this difference was not
statistically significant (P=0.3, one-tailed t-test,
d.f.=4).
Although we hypothesize that mucus on the arches serves to reduce the loss of water between the rakers and between the arches, thereby increasing crossflow speed and inertial lift, a decrease in inertial lift force in the absence of mucus would have to be dramatic to be detectable from particle movement through the endoscopic field of view. Our finding that crossflow filtration continued to operate in the absence of gill rakers and mucus indicates that the surfaces of the branchial arches themselves play an important role in crossflow filtration. Studies are in progress to determine the effects of gill raker removal on particle retention efficiency and particle size selectivity during crossflow filtration in O. aureus.
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Acknowledgments |
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Footnotes |
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* Present address: College of Veterinary Medicine, Virginia Polytechnic
Institute and State University, Blacksburg, VA 24061, USA 
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References |
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