AMER. ZOOL., 36:373-384 (1996)
Gill Structure in Zebra Mussels: Bacterial-Sized Particle Filtration1
HAROLD SILVERMAN, JOHN W. LYNN, ERIC C. ACHBERGER 2 ,
AND THOMAS H. DIETZ
Department of Zoology and Physiology, and ''•Department of Microbiology,
Louisiana State University, Baton Rouge, Louisiana 70803
SYNOPSIS. The filtration mechanics of the gill of the zebra mussel, Dreissena polymorpha, allow this organism to capture particles less than 1 |xm.
The organization of gill cirri and the architecture of the cirri appear to be
important in providing the organism with the ability to filter small particles. Bacteria may provide a useful nutrient source for these animals as
bacterial proteins can be digested and assimilated into mussel proteins.
Laboratory experiments indicate that D. polymorpha is capable of filtering
and assimilating a wide range of bacteria ranging in size from 1—4 u,m.
Unionid species appear to be at least an order of magnitude less efficient
at filtering bacteria than D. polymorpha. Because of its relatively smaller
gill size, C. fluminea also filters bacteria less efficiently than D. polymorpha. We suggest that bacterial utilization by freshwater mussel species
has important population and evolutionary implications.
INTRODUCTION
and 2) laboratory data documenting the utilization of bacteria by these mussels.
The ability of Dreissena polymorpha to
establish large, dense populations and subGILL STRUCTURE
sequently alter the water quality is well
One important clue to the ability of D.
documented (Reeders and Bij de Vaate,
1990; Maclsaac et al., 1992; Stanczykows- polymorpha to utilize bacteria as a nutrient
ka and Lewandowski, 1993). Reports of re- source comes from observation of gill
duced phyto- and zooplankton levels after structure. The gill of D. polymorpha is of
D. polymorpha become established in a the classic eulamellibranch form with two
lake indicate these mussels may impact the epithelial lamellae surrounding a central
planktonic structure in a body of water. This water channel (Fig. 1). The mechanics and
situation presents a paradox. If a mussel re- function of such gills in water movement
duces plankton levels, then how are dense and particle filtration has been generalized
mussel populations maintained or in- across species. J0rgensen (1990) has procreased? We have recently suggested that vided a recent and extensive review of this
part of the answer to the paradox may lie field. In the generalized mechanism, the
in the ability of Dreissena polymorpha to force for water flow is largely generated by
extract and utilize bacteria as a nutrient lateral ciliated cells (J0rgensen, 1990).
source. The purpose of this report is to brief- However, some argue that there is a disly review the experimental laboratory re- crepancy between calculated and experisults indicating 1) physical gill structure mentally measured water velocity and the
which may be related to bacterial capture pressure drop expected in the system driven
solely by lateral cilia (Silvester and Sleigh,
1984; Silvester, 1988). There is indirect ev1
From the Symposium Biology, Ecology and Phys- idence that gill musculature also can and
iology of Zebra Mussels presented at the Annual Meet- does contribute to the regulation of water
ing of the American Society of Zoologists, 4—8 Janu- flow through the eulamellibranch gills (Garary 1995, at St. Louis, Missouri.
diner et al., 1991a). Musculature in the gill
2
Address correspondence to: Harold Silverman, Department of Zoology and Physiology, Louisiana State is organized and positioned to regulate the
size of both the external and internal ostia
University, Baton Rouge, Louisiana 70803.
373
374
H. SlLVERMAN ET AL.
1a
FIG. 1. Cross section (anterior-posterior) of a gill cut perpendicular to the long axis of the gill filaments, (la)
At low magnification the central water channel (WC) is seen between the two epithelial lamellae which are
organized as filaments (F) supported by connective tissue matrix (arrow). Water canals pass between filaments
and open (arrowhead) into the water channel. A connective tissue/muscle septum (S) joining the two filaments
is seen between adjacent water channels. Higher magnification of a single filament (lb) shows ciliary organelle
USE OF BACTERIA BY DREISSENA
of the water canals through which water
will flow (Gardiner et al., 1991a, b; Tankersley and Dimock, 1993; Medler and Silverman, 1994). Furthermore, Gardiner et al.
(1991a, b) showed that serotonin relaxes
the musculature associated with the internal
and external ostia of the water canals in
unionids. Tankersley and Dimock (1993)
observed rhythmic movements of the
unionid demibranch using video endoscopy.
Similar musculature has recently been described for D. polymorpha gill (Medler and
Silverman, 1994). The neuromuscular
agent, serotonin, has been shown to cause
expansion of the ostia, presumably by muscle relaxation, and both FMRFamide and
acetylcholine cause ostial musculature to
contract (Medler and Silverman, 1994;
Duncan et al., 1994). Monographs on the
marine genera, Pecten (Setna, 1930) and
Ostrea (Elsey, 1935), indicate muscular
anatomy in the gill consistent with muscular regulation of water flow through the gill.
Located more toward the apex of the filament, with reference to the lateral ciliated
cells, are latero-frontal cells that possess
more specialized structures that are usually
composed of paired and fused ciliary sheets
known as cirri (Fig. 2). These cirri are
found on many bivalves, both freshwater
and marine, and similar organelles are present in other invertebrates. Atkins (1938)
suggested that their presence or absence
could be used as a characteristic to classify
bivalves. However, the wide variation in
cirral structure amongst bivalves has not
been particularly useful for classification
purposes. Cirri are described by some authors as forming a physical filtration net
used to trap particles from the water column
(Owen, 1974; Owen and McCrae, 1976).
Others indicate that particles are not filtered
375
by physical structures but are captured by
complex water currents created by the sum
of all ciliary movements of the filaments
(J0rgensen, 1981a, b; J0rgensen, 1990;
Ward et al, 1993; Nielsen et al., 1993).
Some of the controversy between these
opposing views has been attributed to observations of fixed material or of gills that
have been excised from the animal (Ward
et al., 1993). Those researchers favoring
water currents as a mechanism argue that
information obtained from such altered systems is not particularly useful. Clearly, observations of fixed gill material are of value, but can be flawed by systematic error,
including differential shrinkage, alteration
of structures and their position during fixation, and the inability to observe the various forces acting on the gill in the living
condition. Dreissena polymorpha gill is
particularly susceptible to osmotic shock.
Variation in fixative or buffer solutions by
as little as 10 mOsm from being isosmotic
with the hemolymph causes severe disruption of the tissue in D. polymorpha (Fig. 3).
This finding is in complete agreement with
the physiological sensitivity of the animal
to sudden changes in osmolarity (Dietz et
al., 1994, 1995). The other source of controversy lies in the attempts to overgeneralize and create a single mechanism for the
diverse bivalve species. Broad generalizations have proven useful, but like any model, they need to be viewed in context and
with a healthy regard for the variation between gills from various species. For instance, some gills produce relatively little
mucus on their gill filaments and have few
mucus producing cells in their filament epithelium (D. polymorpha); whereas, others
show extensive mucus production {e.g., Carunculina texasensis, Anodonta grandis).
position. The frontal cilia (F), are located at the apex of the filament, latero-frontal cirri (C) are below the frontal
cilia, and lateral cilia (L) lie between adjacent filaments above the ostia (arrowhead) leading to the water canal.
The white arrowhead depicts the viewing angle for Figures 5a—e. Bar (la) = 50 u.m; (lb) = 25 u.m.
FIG. 2. Transmission (2a), scanning (2b), and laser confocal (2c) micrographs showing cirri structure. Cirri are
composed of fused individual cilia. The base of the cilia makes up the fused portion of the cirral (cirral body,
B). The tips of the individual cilia (T) are not fused and the tips are thinner than the basal body portion of the
cilia. The confocal micrograph is frame frozen and isolated from a time series (30 frames/sec). The scanning
micrograph shows an abrupt shoulder region marking the end of the cirral body and the beginning of the free
tip region. Bars (2a) = 2 u,m; (2b) = 2 u,m; (2c) = 5 u.m.
376
H . SlLVERMAN ET AL.
FIG. 3. Electron micrographs of gill tissue fixed in hyper- and hypoosmotic fixative. (3a) a gill filament fixed
using 50 mOsm phosphate buffer. Compare the shape of this filament to those seen in Figure 1. Latero-frontal
cells (C) have not shrunk as much as frontal cells (F), lateral ciliated cells (L), and the indifferent epithelial
cells which lie between Iatero-frontal cells and lateral cells. The indifferent epithelial cells display abnormal
cytoplasmic processes (P) extending from the filament. (3b) is fixed only in glutaraldehyde in pondwater with
USE OF BACTERIA BY DREISSENA
The abundance and type of mucus at the
gill filament capture site could be a source
of important differences in particle capture
mechanics. Moreover, particle capture is a
separate phenomenon from particle transport. Recent observations based on endoscopic work provide valuable information
on particle transport mechanisms but more
limited information on particle capture because of the resolution limits of the technique (Ward et al, 1991, 1993; Beninger et
al, 1992).
Recent observations using laser confocal
microscopy, with its attendant high resolution, of living gills of Dreissena polymorpha indicate that cirri are important to the
overall particle clearance mechanism. Cirral
interaction with particles may be particularly important for small particles in the range
of 1 |xm (Silverman et al, 1996). It should
be noted that the confocal microscopic observations have been made on living excised tissue, meaning that all forces existing
in vivo and influencing particle capture
mechanisms were not maintained in the
preparation.
Thus, the two recent advances in microscopy that have contributed to the debate on
the mechanism of particle filtration by bivalves gills are endoscopy to observe gills
in intact animals (Beninger et al., 1992;
Tankersley and Dimock, 1993; Ward et al.,
1991, 1993, 1994) and laser confocal microscopy (Silverman et al., 1996). The advantage of video endoscopy observations is
that the gill tissue remains intact in the animal allowing observation of the gill and its
311
mechanics with minimal disruption. The
major contribution of video endoscopy has
been a refining of the gross particle movement patterns exhibited by the gills and
palps of several bivalve species. The disadvantage of video endoscopy is that the
resolution obtainable with current technology is limited to about 5 u.m (Ward et al.,
1994) and many of the events involved in
particle capture, especially those in the 1
(Jim size range, cannot be directly observed.
The value of laser confocal microscopy is
that the resolution limit is in the sub-micron
range. Furthermore, the depth of field is selectable, allowing the mechanics of cilia
and cirri to be directly and individually observed and analyzed. However, while living
gills can be observed in vitro with confocal
microscopy, the technique cannot be used
in situ.
The beat of D. polymorpha cirri (Fig. 4)
has been described as a motion that brings
the cirri up over the apex of the filament in
the flexed position, and into an extended
position across the interfilament space (Silverman et al., 1996). In the straight or extended position, the free tips of the cirral
cilia spread across the interfilament space
forming a net with spacing of approximately 0.2-0.7 |xm (Silverman et al, 1996).
This size range and structure of the cirri
clearly suggest low Reynolds number fluid
mechanics. The characteristics of single fiber and more complex biological filters in
particle interaction and capture under
steady state (or creeping flow for low Reynolds number) has been modelled both nu-
no buffer. In this case water channel (WC) epithelium has sloughed from the underlying connective tissue
(arrows) leaving a naked basement membrane. This was a commonly observed artifact associated with hypoosmotic fixation. Bars (3a) = 5 u.m; (3b) = 5 u,m.
FIG. 4. Scanning electron micrographs illustrating cirral position in fixed gill tissue. (4a) High magnification
showing the structure of the "capture net." The free tips of the cirri (arrow) form the net. Note the cirri from
two filaments are observed. At the top of the micrograph the cirri are fully extended. The cirri from the adjacent
filament are also almost fully extended. The most distal section of these cirri are positioned slightly above the
first set of cirri, (taken from Silverman et al., 1996) (4b) Lower magnification of two adjacent filaments showing
the position of the cirri relative to the frontal cilia (F). Sets of extended cirri (arrowhead) are adjacent to cirri
in the flexed position (arrows) indicating the cirri are in different beating positions as would be expected along
a length of filament, (taken from Silverman et al., 1996) (4c) and (4d) are higher magnification of cirri in the
flexed or bent position. In both micrographs, note the interaction of the tips of the cirri with bacteria. In (4c)
the bacteria are Bacillus megaterium (M) and in (4d) the bacteria are Escherichia coli (arrowheads). Note such
images provide no evidence for cirri capture of bacteria, but do show relative sizes. Bars (4a) = 5 jtm; (4b) =
20 u.m; (4c) = 2 u.m; (4d) = 10 \s.m.
378
H. SlLVERMAN ET AL.
FIG. 5. (a-e) Laser confocal images of live Dreissena
polymopha gill representing a time series captured on
video (30 frames/sec). For orientation purposes, 5f is
a bright-field photograph of a video captured image of
the frontal surface of filaments (FS) on a living gill
preparation. The interfilament space (IS) is indicated.
The area in 5f similar to that depicted in the confocal
micrograph series is outlined within the white box. The
top of the focal plane in 5f is below the frontal cells
of the filament. The depth of field in 5f includes most
of the cirral cells and the cirral bodies (arrowhead) are
visible in the interfilament space. A few of the cirri
show the V's (white arrowhead) formed by the flexible
ciliary tips as the cirri bend into the flexed position
approaching the frontal surface. The frontal surface of
a filament (FS) is located at the top of each confocal
image (5a-e) and corresponds to the edge of FS in 5f.
Most of the individual cilia on the frontal surface are
out of the confocal plane, but part of the tips of a few
frontal cilia are visible. Cirri are visible on one side of
this filament. The beat of these cirri results in a flexion
into the plane of focus and over the frontal surface.
During extension the cirri move down and slightly to
the left out of the plane of the section into the interfilament space. The free cilia tips of each cirrus form
a fluorescent "V" as it is flexed over the front of the
filament (see Figs. 4b and 5f). The width of the open
face of these V's is approximately 2 p.m. The dark
space below the bright V's is the interfilament space,
and when the cirri are extended they drop down and
out of the visible plane. The bright lines at the bottom
of each image are the cirral bodies of the adjacent
filament located below the bottom of each of the images. The major differences between confocal (5a-e)
and brightfield (5f) are the smaller depth of field and
the greater resolution in the confocal images. The observation angle is also shifted more toward the edge
of the frontal surface of the filament than in 5f (the
angle of view indicated by the white arrow in Fig. lb).
The bright dot on each image is a 0.75 jim fluorescent
particle (arrowhead), one of many which were added
to the preparation and allowed to move across the gill.
The particle was floating freely at the beginning of the
time series. In (5a) the particle (arrowhead) is moving
USE OF BACTERIA BY DREISSENA
merically and experimentally {e.g., reviews
by Rubenstein and Koehl, 1977; Shimeta
and Jumars, 1991). Such models predict
that cirri behave as paddles and not as physical sieve devices (Rubenstein and Koehl,
1977; Shimeta and Jumars, 1991). However, for the gill of Mytilus edulis, Nielsen et
al., (1993) suggest from partial model systems that the interfilament area of the gill
is not strictly in a steady flow state due to
the velocity differences in this region
caused by the ciliary pump. Shimeta and
Jumars (1991) suggest that under nonsteady state conditions particle movements
and interaction with filter elements may
vary considerably from that predicted by
steady flow modelling.
Observations made using confocal microscopy confirm that cirri trap or (perhaps
the better phrase is) deliver 0.75-1 u,m fluorescent beads (Silverman et al., 1996) to
the frontal surface of the gill. The delivery
of a 0.75 (Jim particle by a cirrus onto the
frontal surface of the filament is shown in
the time-lapse images captured using laser
confocal microscopy (Fig. 5). These images
by themselves do little to confirm whether
the delivery mechanism is strictly hydromechanical or whether some particle contact with the cirri occurs. Given the unsteady flow environment, only exacting
below the front of the filament. In (5b) a cirrus (arrow)
is flexing into the plane pushing the particle up onto
the frontal surface of the filament. In (5c) the cirrus is
fully flexed and the particle is up on the filament. In
(5d) the particle (arrowhead) has begun to move to the
right across the frontal surface and continues to do so
in (5e). In the next images (not shown) following this
series the particle became entrained in the frontal cilia
water flow and accelerated as it moved across the frontal surface at a speed of 50 fim/sec along the frontal
surface of the filament. This time series also indicates
the beat pattern of the cirri on a gill filament generally.
The beat pattern is such that some cirri are flexing
while others are extending. All of these cirri were beating rapidly and the average beat cycle was about 15
Hz for an individual cirrus. The time series represents
a reasonably good preparation with spontaneously
beating cirri. The movement of the particle along the
frontal surface reflects good frontal ciliary beat, although that is not directly visible in this set of images.
Finally, a few of these images suggest the presence of
pro-lateral-frontal cilia (white arrow in 5d). Bars (5a—
e) = 2 u,m; (5f) = 4 u.m.
379
measurements of fluid velocities at the cirral sites themselves, identification of particle trajectories at these sites, and measurement of shear and/or drag forces will allow
the exact mechanism of cirral interaction
with particles to be determined. What does
appear to be clear from the data presented
in Nielsen et al. (1993) for Mytilus and for
our confocal observations of Dreissena is
that there is a close interaction between gill
cirri and particles. The ability of a species
to efficiently capture small particles does
appear to correlate with the complexity of
cirri as reported in many comparative studies among bivalves (Owen and McCrae,
1976; Vahl, 1973; McHenery and Birbeck,
1985; M0hlenberg and Riisgard, 1978;
Riisgard, 1988; Silverman et al, 1995).
We have also observed the rapid movement of large numbers of particles in the
frontal current as described by various investigators. These morphological observations led us to conduct experiments to determine whether or not bacteria are effectively cleared by D. polymorpha.
CLEARANCE OF E. COLI BY D. POLYMORPHA
AND OTHER FRESHWATER BIVALVES
Sprung and Rose (1988) report that D.
polymorpha can filter particles in the 0.7
|j,m range, but that these particles are not
efficiently handled. J0rgensen et al. (1984)
indicate that particles as small as 1 u,m are
filtered by D. polymorpha with over 90%
efficiency, an efficiency similar to that for
larger particles up to 8 p,m in diameter. Finally, Morton (1971) documents a two-fold
greater assimilation of bacteria over algae
by Dreissena. In our laboratory, in experiments designed to examine uptake of bacteria by mussels, we utilized 3-5 X 107 bacteria/ml. To do this, Escherichia coli were
labelled with 35S and fed to Dreissena polymorpha (Dreissenidae), Carunculina texasensis (Unionidae), and Corbicula fluminea {Corbiculidae). The ability of these
mussels to remove or clear bacteria from
the water column is shown in Figure 6 (Silverman et al., 1995). The data in Figure 6
are normalized to dry tissue weight, but we
have also analyzed the data both with reference to the surface area of the gill and the
number of cirri per gill surface area (Sil-
380
H. SlLVERMAN ET AL.
•§j 0.9| 0.8£ 0.7•2 0.6 :
% 0.5 :
•° 0.4° 0.32 0.H
"-o.o
0
i
102030405060708090
Time, min
FIG. 6. Time dependent removal of E. coli from
pondwater by D. polymorpha (filled square), C. fluminea (square), or C. texasensis (circle). Each mussel
was placed in 20 ml of pondwater containing 6 X 108
bacteria labelled with 35S. Each point represents the
mean ± SEM for at least 10 separate animals. The
curves represent exponential decrease or removal of
bacteria from the water by each species. The t1/2 was
10.2, 12.0, and 62.7 min for D. polymorpha, C. fluminea, and C. texasensis, respectively. The clearance
rates in ml (g dry tissue • min)"1 for the 3 species was
143, 4.4, and 1.3, respectively (taken from Silverman
et al, 1995).
verman et al., 1995). The unionid, C. texasensis, has the least developed gill cirri
and also showed the least ability to filter
bacteria from the water column. Further experiments on D. polymorpha indicate that
filtration was dependent on bacterial concentration (Silverman et al., 1995). The
choice of 35S over 3H or 14C as a tracer eliminates the problems of isotope exchange
(protons for 3H) and respiratory loss of
I4
CO2.
Filtration by itself does not indicate utilization of the bacteria as a nutrient source.
However, analysis by gel electrophoresis
(Fig. 7) (Silverman et al., 1995) indicates
that bacterial protein is digested and labelled amino acids are incorporated into
mussel protein by D. polymorpha. We determined the amount of 35S incorporated
into mussel protein compared to the total
amount of 35S-labelled bacteria disappearing from the bath to provide an estimate of
26% efficiency for incorporation of label
into mussel protein for the three species
tested. Interestingly, mussels collected from
E
F
FIG. 7. Autoradiograph of a 12%-polyacrylamide gel
loaded with protein isolated from the homogenized
whole body of D. polymorpha. Mussels were allowed
48 hr to assimilate 35S-labelled E. coli after a 20 min
feeding experiment (individual mussels represented in
lanes A-E). Lane F represents the solubilized protein
fraction of the 35S-labelled E. coli used in the feeding
experiments. Molecular weight markers were located
from the stained gel. Note the similarity in band pattern between individual D. polymorpha (lanes A—E)
and the distinctive difference between these lanes and
the E. coli protein in lane F. There was no evidence
for the presence of any of the recognized E. coli proteins in the D. polymorpha lanes (the heavy E. coli
bands at about 50 kDa and 95-100 kDa were not present in lanes A-E). Conversely, many of the major labelled proteins in the mussel tissue do not appear in
the E. coli band (adapted from Silverman et al., 1995).
the Mississippi River and tested immediately (<24 hr in the laboratory) showed no
difference in the rate of bacterial clearance
when compared to animals acclimated in
the laboratory for weeks. These data are in
agreement with those of Morton (1971) indicating substantial utilization of bacteria
by D. polymorpha. Finally, D. polymorpha
was provided five different laboratory bacterial species ranging in size from 1-5 |xm.
All of these organisms were successfully
cleared from the water by D. polymorpha
(see Silverman et al., 1995).
USE OF BACTERIA BY DREISSENA
As in many other bivalve species, particle filtration rates are dependent on the particle concentration in the water column. Our
bacterial filtration experiments indicated an
optimal particle concentration at about
1.5 X108 bacteria/ml, much higher than that
found for algal cultures (Morton, 1971;
Walz, 1978). Our data are nearly identical
to those first reported by Mikheev and Sorokin (1966) for bacteria ranging between
0.4 and 1 u.m in diameter. Morton (1971)
notes that as the size of the algal food particle increases the number of cells which
promotes optimal filtration is reduced.
Maximal filtration of various algal species
range from 40 to almost 105 cells/ml. Similarly, Dorgelo and Smeenk (1988) report
maximal filtration of Chlamydomonas at a
level somewhat below 105 cells/ml. However, these investigators report that all mussels given this concentration of algae died.
Chlamydomonas (and other alga) culture
media are designed to produce large numbers of algae in a short period and are high
in potassium. Excess potassium rapidly enters the mussels and causes extreme physiological changes in Dreissena including
death (Fisher et al, 1991; Dietz et al,
1994; Wilcox and Dietz, 1995). Experiments with D. polymorpha using media
where ionic balances (especially K) are not
carefully managed will stress the animals.
Such ionic imbalance could account for
much of the variability in feeding and filtration experiments incorrectly attributed to
a general laboratory "disturbance" factor.
DISCUSSION
Reports documenting or calculating a reduction in phytoplankton in the Great Lakes
are numerous (Maclsaac et al., 1992; Bunt
et al., 1993; Leach, 1993), yet the population densities being reported for D. polymorpha have not declined in many of these
same locations. For the mussels to remain
at densities of 105-106/m2 requires that they
have a reasonably stable food source, yet
indications are that the usual and suspected
food sources have declined dramatically as
zebra mussel populations have stabilized.
The information reviewed here clearly demonstrates that D. polymorpha can assimilate
bacterial nutrients into bivalve protein, at
381
least in these laboratory experiments (Silverman et al., 1995). Mikheev and Sorokin
(1966, cited in Morton, 1971) report that
assimilation of ingested algae is only 40%
of bacterial assimilation by D. polymorpha.
Similarly, in the marine environment,
oyster beds, through filtration of plankton
and subsequent production of feces and
pseudofeces, are known to change nutrient
distribution (C, N, and P) in local environments (Dame et al., 1984). These changes
lead to enhanced production of bacteria
(Kemp and Boynton, 1984). Crosby et al.
(1990) also report that Crassostrea virginica can derive some of its nutrients from
bacteria. Similar interactions with other marine bivalve species are reported by numerous authors, as reviewed recently by Prieur
et al. (1990).
Pseudofeces and feces are evident at field
sites in association with zebra mussel accumulations, and production of pseudofeces
is observed following exposure of D. polymorpha to artificial diets, including monospecific algal cultures and/or dried algae.
Each D. polymorpha (1-2 cm length)
moves 1-4 liters of water per day and has
the capacity to filter diatom- and phytoplankton-sized particles at almost 100% efficiency (J0rgensen et al, 1984). Pseudofeces will be produced under many circumstances including when particles are in excess of nutrients required. Reeders and Bij
de Vaate (1990) indicate that as D. polymorpha colonizes a lake they reduce nutrients in the lake by filtration and deposition
of feces. Thus, nitrogen and phosphorous
are transferred from the water column into
the sediment. We suggest that these nutrient
distribution changes are occurring, and that
prokaryotes are able to take advantage of
the nutrient redistribution. Thus, D. polymorpha may be capable of using the bacterial flora present in the mussel bed as a
food source (Silverman et al., 1995).
Field experiments on the microbial populations associated with D. polymorpha
beds are required to verify that the proposed
mechanisms are actually operating in natural water systems. Studies have indicated
that bacteria alone are not sufficient for
growth of these mussels (S. J. Nichols, personal communication). For instance, the
382
H. SlLVERMAN ET AL.
bacteria appear to be lacking some fatty ac- freshwater an opportunity to exploit an adids essential to the mussel. However, we are ditional resource not being utilized by the
not postulating utilization of bacteria as a unionids, and to occupy areas unavailable
sole nutrient source. Rather, we suggest that to the unionids. A modern equivalent which
bacteria can make up one component of the may mimic this condition is that Corbicula
nutrient pool utilized by D. polymorpha.
fluminea are often found in areas that are
That D. polymorpha and Corbicula flu- seemingly too poor in phytoplankton to
minea feed on bacteria may have contrib- maintain unionid populations (McMahon,
uted to the ability of these organisms to in- 1991). Byrne et al. (1995) demonstrate that
vade freshwater during or shortly before the at least over the short term and for unionids
beginning of the Pleistocene (McMahon, encrusted by as many as 100 D. polymor1991). The unionids as a group have been pha, that suffocation is not occurring, and
highly successful in freshwater since the that perhaps starvation is the more imporTriassic, as evidenced by the fossil record tant of the short-term negative impacts of
and the tremendous radiation of species Dreissena polymorpha on the unionid popthroughout the world. Thus, additional bi- ulations of North America.
Field experiments designed to assess bacvalve groups successfully migrating into
freshwater needed to be able to avoid, com- terial colonization of D. polymorpha beds,
pete or perhaps outcompete the unionids al- comparative laboratory studies of the abilready present. As mentioned above, bacte- ity of several unionid species with varying
rial filtration by Carunculina texasensis was cirral structure to utilize bacteria, and comsignificantly less than either D. polymorpha bined algal/bacterial studies aimed at deteror C. fluminea. A comparison of the cirral mining differential assimilation by D. polystructure of these three species indicates morpha and C. fluminea are. all required to
that both D. polymorpha and C. fluminea evaluate the hypotheses presented here.
have approximately 33-42) cilia per cirral
ACKNOWLEDGMENTS
plate, while C. texasensis has only 11-12
cilia per plate (Silverman et al., 1995).
The authors thank Julie Cherry and Ron
There is wide variation among unionid spe- Bouchard for their excellent technical assiscies with regard to cirral structure. For ex- tance. We also thank S. Jerrine Nichols and
ample, several unionids (e.g., Ligumia na- Kevin Carman for thoughtful discussion.
suta and Anodonta imbecilis) have struc- The morphological studies were conducted
tures similar to C. texasensis, and a few of in the College of Basic Sciences Microsthe unionids have more developed cirri with copy Facilities. Our laboratory was supcilia number approaching 36 (e.g., Ptycho- ported by Louisiana Sea Grants R/ZMbranchus fasciolaris) (S. J. Nichols and H. 1-PD and NA46RG0096 project R/ZMM-1.
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