You are on page 1of 8

Rus,~ian Journal of Marine Biolog3; VoL 26. No. 2, 2000. pp. 81~88.

Original Rus,~ian Text Copyright 9 2000 by Biologiya Morya, Govorin.


E C O L O G Y
Rol e of Bi val ves in the Depurat i on of Seawat ers
Cont ami nat ed by Bact eri a
I . A. G o v o r i n
Odessa Branch, Institute of the Biology of Southern Seas, National Academy of Sciences of the Ukraine,
Odessa, 270011 Ukraine
Received January 11, 1999
Abst ract --Bact eri al contamination the inshore areas of seas, is currently one of the most common manifesta-
tions of increasing anthropogenic pressure on aquatic ecosystems. Permanent sources of allochthonic microf-
lora in the inshore areas of seas, are polluted with untreated or insufficiently treated domestic and industrial
sewage [5, 8, 12, 45, 66] and river run-off from areas of active water use [22, 28], and suffer the effects of over-
exploitation of beaches during the bathing season (in the summer).
In recent years, hi gh l evel s of bact eri al cont ami na-
t i on of mar i ne wat ers have been det ect ed in vari ous
r egi ons of t he worl d, i ncl udi ng t hose pr evi ousl y
t hought to be ecol ogi cal l y safe [63].
Unde r t hese condi t i ons, it has be c ome i ncr easi ngl y
i mport ant to st udy the nat ural puri fi cat i on of sea wat ers
and the sani t ary rol e of sel ect ed speci es of aquat i c
or gani sms, part i cul arl y bi val ves, whi ch are a mong t he
most act i ve filtering organi sms. Becaus e of t hei r unsat-
i sfact ory sani t ary and hygi eni c charact eri st i cs, many
i nshor e areas of t he seas are becomi ng unsui t abl e for
mol l usk mari cul t ure. Consi der i ng t he st eady loss of
ecos ys t ems wi t h l ow bact eri al pressure, t he cur r ent
strategy of bi val ve mar i cul t ur e needs t o be changed. In
particular, c ommon speci es of mol l usks are pot ent i al l y
very useful in the bi oamel i or at i on of t he mar i ne envi -
r onment [48]. However , t he sani t ary and bact er i ol ogi -
cal rol e of mar i cul t ur e farms must be compr ehens i vel y
and t hor oughl y st udi ed.
In this revi ew, at t ent i on is f ocused on the mi cr obi o-
l ogi cal aspect s of t he i nt eract i ons of bi val ve mol l usks
and t he envi r onment .
Efficiency o f Retention and Accumulation
o f Microorganisms by Mollusks
The hi gh filtration capaci t y of bi val ves was demon-
st rat ed as earl y as t he 1920- 1940s by a number o f
i nvest i gat ors [7, 17, 44, 50]. Ther e are a vari et y of opi n-
i ons as to the part i cl e sel ect i vi t y and filtration ef f i ci ency
of mol l usks. J r r ge ns e n [ 50- 53] showed that s ome
bi val ves effi ci ent l y ret ai n part i cl es of a f ew mi crons.
Haven and Mor al es - Al amo [47] f ound that t he oyst er
Crassostrea virghlica ret ai ns 1-3 lam part i cl es wel l ,
al t hough the filtration ef f i ci ency is less t han 100%.
Spi t t l er et al. [73] showed that t he oyst er C. rhizo-
phorae ret ai ns food part i cl es of a wi de size range, pre-
ferri ng part i cl es f r om 25 to 56 lam, al t hough it al so
i ngest s very smal l part i cl es of less t han 1 l i m in di ame-
ter. The mol l usk Solen cylindraceus ret ai ns 70- 90% of
sest on part i cl es of 2. 5- 3 ~tm; bel ow t he size of 2 pm, its
filtration ef f i ci ency is mar kedl y r educed [80]. In t hei r
cl assi c wor k on t he filtration of vari ous suspensi ons by
t he mussel Mytilus edulis, Tammes and Dral [77]
emphas i ze that ret ent i on ef f i ci ency is pr i mar i l y rel at ed
t o part i cl e size. In l i ne wi t h this obser vat i on, t he
aut hors i dent i fy a size gr oup of part i cl es ( 7- 8 lxm) t hat
are ful l y r et ai ned by t he mol l usk and a group of smal l er
part i cl es that t he mussel is unabl e to ret ai n dur i ng one
pr opul si on of wat er t hr ough its gill apparat us ( 1. 5-
2.5 l.tm fragel l at es and bact eri a).
Thus, a number of aut hors have poi nt ed out that
mol l usks can capt ur e part i cl es l arger t han 2- 3 lam, as
wel l as part i cl es of I - 3 / a m and smal l er [64, 65, 67].
This particle size range mat ches the cel l di mensi ons of
various aut ocht honous mari ne mi croorgani sms and
col i f or m bacteria, whi ch are universal indicators of
ant hropogeni c pollution of t he aquatic envi r onment [ 14].
Dat a on t he ret ent i on effi ci ency of vari ous mi croor-
gani sms by bi val ves are ambi guous and somet i mes
cont roversi al . On t he one hand, the occur r ence of
di ver se al i ocht honi c mi cr of l or a in mol l usks, i ncl udi ng
i ndi cat or y and pat hogeni c ent er i c bact er i a such as Bac-
terium coli, Salmonella and Shigella sp, Vibrio chol-
erae, and V. parahaemolyticus has been wel l docu-
ment ed for cont ami nat ed sea areas [4, 20, 24, 36, 37,
62]. In a number of count r i es, eat i ng r aw or insuffi-
ci ent l y t her mal l y pr ocessed mol l usks has been report ed
to cause shellfish poi soni ng [15, 34, 43, 60]. On the
ot her hand, t he mechani s m of ret ent i on of bact eri a by
bi val ves, its effi ci ency, and pr i mar i l y t he f ur t her fat e o f
capt ur ed bact eri al cel l s r emai ns t o be st udi ed.
1063-0740/00/2602-0081 $25.00 9 2000 MAIK "Nauka/lnterperiodica"
82
GOVORIN
Efficiency of Removal by Mollusks of Microbial Cells
from Bacterial Suspension
A number of authors have noted the low percent
retention by mollusks of solitary bacterial cells from
suspension. The oyster Ostrea virginica is only able to
retain a small part of the bacteria B. coli (1.1-1.5 x 2. 0-
6.0 ~tm) added to native seawater, while 70-90% of the
bacteria avoid passing through the gills, and can be
found only in water filtered out by mollusk [44]. The
retention efficiency of bacteria by the mussel M. edulis
in experiments using microbial cells of 0.5-2.5 ~tm was
in the range from 5 to 24% [77]. However, the authors
remark that the results are based on only ten observa-
tions performed with a limited number of animals.
As early as the 1930s, it was noted that mussels
actively settle out suspensions of bacterial cells and can
live for a long time without any other food [82].
McHenry and Birkbeck [6l] demonstrated that
M. eduIis, O. edulis, and Mya arenaria capture even
solitary bacterial cells from suspension, while the mol-
lusk Chlamys opercularis can only do so from the algo-
bacterial mixture of Escherichia coli and Tetraselmis
suecica. The addition of the latter to cultured microor-
ganisms enhances the filtration rates by M. edulis and
O. edulis. It is the rate but not the efficiency of filtration
that increases, since E. coli cells do attach to the algae.
For many bivalves such as Cardium echinatum,
Modiolus modiolus, and Arctica islandica, particles of
up to 1 lam are not limiting. However, most autochtho-
nous bacteria are less than 1 lam in diameter; therefore,
the clearance efficiency of these bacteria is not above
20-30%. Nevertheless, some mollusks, such as Geu-
kensia demissa, are able to retain bacteria of 0.2-0.4
and 0.4--0.6 ktm with an efficiency of 30 and 86%,
respectively. The removal efficiency of cyanobacteria
and some other bacteria by these mollusks varies from
25 to 56% per hour. It has also been noted that bacteria
are not retained, as well as medium-sized living phy-
toplankton organisms or flakes of organic material (up
to 95%), although the removal efficiency of particles is
not dependent solely on particle size [55].
Laboratory measurements of filtration of natural
marine bacterioplankton by the mollusks M. edulis and
M. arenaria indicate that bacteria of more than 0.5 lam
in size are removed more efficiently [81]. In experi-
ments, the mollusk Venus verrucosa assimilates about
14
60% of C -labelled Lactobacillus sp. added to native
seawater. The highest amount of C14was found in the
visceral tissue, gills, and mantle when expressed based
on dry weight in the gills [31].
The Black Sea mussel Mytilus gaUoprovincialis was
found to remove a large quantity of allochthonic bacte-
ria from native seawater experimentally contaminated
by domestic sewage [10]. At optimal temperature and
salinity (18~ and 15 to 16%0) and active water motion,
the removal rate of bacteria from suspension was 6.4 x
104-2.0 x 107 cells/(ind h) for 17-18 mm mussels and
7.6 x 105-1.6 x l 0 s cells/(ind h) for 55-60 mm mussels.
Mussels eliminated 54.5-71.0% of the heterotrophic
bacteria and 68.0-76.0% of the enteric bacteria from
the water mixture. The average values of elimination
were 38. I-59. 6% for I 7- 18 mm mussels and 49. 9-
63.6% for 55--60 mm mussels.
It should be noted that, for filter-feeding organisms
such as bivalves, along with the concentration of bacte-
rial cells, the degree of their aggregation is important in
the retention of microorganisms captured from the
environment. Sorokin et al. [26, 27] showed that 30 to
40% of natural bacterioplankton cells are united into
aggregates of more than 4 ktm in size and, being aggre-
gated, are easily captured even by coarse filtering
organisms such as mussels and oysters.
Experimental studies have demonstrated that the
adsorption of bacterial cells is directly related to mol-
lusk species and environmental temperature. Almost all
authors point out that seawater temperature largely
affects the physiological activity of bivalves and, as a
consequence, the efficiency of accumulation of bacte-
ria. For four species of bivalves (M. arenaria, Pro-
tothaca staminea, Crassostrea gigas, and Mytilus edu-
lis), a positive correlation between the uptake of
coliform bacteria and temperature has been found.
Mussels more intensively accumulated bacterial cells at
17~ than at 7-12~ while, for the other three species
of mollusks, the accumulation peak was at 12~ and
the intensity of cell capture was markedly reduced at
17~ Thus, the accumulation of bacteria varies with
season [32], and, moreover, in the mussel M. gallopro-
vincialis, this process is favored by the decreased salin-
ity and increased turbidity of seawater [31 ].
At the same time, there is no consensus in the liter-
ature on the effect of the concentration of bacteria on
mollusks retention efficiency. Some authors believe
that the uptake of bacterial cells by molllusks has a spe-
cific threshold, which is a function of the concentration
of bacteria in water, and that environmental contamina-
tion is positively correlated with the bacterial contami-
nation of mollusks. Cabelli and Heffeman [35], who
studied the accumulation of E. coli by Mercenaria mer-
cenaria, demonstrated that the relationship between
mollusk contamination (y) and the concentration of
bacteria in seawater (X) is described by the equation y =
0.96X + 0.97. A similar correlation was found for the
mussel M. galloprovincialis from the Mediterranean
Sea [31]. However, a f ai r y weak relationship between
the adsorption of coliform bacteria and their concentra-
tion in seawater was found for four species of bivalves,
M. edulis, C. gigas, M. arenaria, and P. staminea [32].
Experiments on artificial contamination of mollusks
have demonstrated that the uptake of bacteria is the
highest at the initial stage, within the first 2--6 h of fil-
tration. Thus, in one study, the mussel M. edulis
removed 90% of H3-thymidine-labelled E. coil, Staphy-
lococcus aureus, Micrococcus luteus, M. cereus, and
Bacilus cereus cells within 2 h [33]. According to Ber-
nard [32], the initial period of the most intensive accu-
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 26 No. 2 2000
ROLE OF BIVALVES IN THE DEPURATION OF SEAWATERS 83
mulation of coliform bacteria by M. edulis is 3 to 4 h.
In addition, there is evidence that the maximum content
of enteric bacteria in this mollusk is already observed
after 30 min of experimentation. It has been empha-
sized that this accumulation efficiency of bacterial cells
is directly related to the concentration of bacteria in
seawater, which, in the study in question, varied from
4 x 101-3 x 107 cells/ml (cited after [70]).
A study of the filtration of the enteric bacteria E. coli
by V. verrucosa showed that, within the first 4 h of
experimentation, the mollusk removes 47.3% of the
cells, while, during the subsequent 20 h, the concentra-
tion of bacteria gradually declines, reaching a plateau.
For the Mediterranean mussel M. galloprovincialis, the
removal efficiency of E. coli cells in the initial 4-h
period is still higher, at 96.6% [39]. In C. virginica and
Mercenaria campechiensis placed in an experimental
unit, the maximum amount of the bacteria Vibrio
vulnificus and V. cholerae is non-observed after 6 h of
experimentation [72]. The oyster C. gigas decreases the
concentration of C~4-1abelled natural bacterioplankton
almost by half within the first 1.5 h of experimentation,
but the filtration rate drops drastically later on [26]. At
the same time, there is evidence that the initial stage of
rapid accumulation of bacteria by mollusks, oysters in
particular, is protracted. Thus, in experiments with oys-
ters artificially contaminated with p32 and Ig~
cultures of enteric bacilli, the maximum uptake of bac-
teria by oysters occurred within i 8 h and declined grad-
ually over the next two days. The uptake efficiency was
dependent on the temperature and salinity of the seawa-
ter [76].
After the fairly intensive initial stage of adsorption
of bacterial cells, this process can be retarded, levelling
off to a plateau, when it is compensated for by the
digestion or elimination of intact bacteria via feces or
pseudofeces [32].
Localization of Bacterial Cells
and Their Subsequent "Fate"
Bacteriological analyses indicated that the degree of
contamination varies among bivalve organs, suggesting
the irregular distribution of absorbed bacteria within
the bivalve body. In mussels and oysters, the contractor
muscle, mantle, and gills are, as a rule, the least con-
taminated, while the highest number of bacteria is
found in the organs connected with food digestion--the
gut and hepatopancreas [38, 56, 64]. Specifically, in the
mussel M. edulis, 75 to 95% of the bacteria are local-
ized in the digestive tract and stomach, while the man-
tle, gills and other tissues, which make up 80% of the
body mass, contain a small number of bacterial ceils
[70]. In the oyster C. gigas, almost 90% of the het-
erotrophic bacteria and up to 93% of the coliform
microorganisms captured from the environment are
found in the digestive tract, mainly in the stomach and
hindgut. Coliforms usually accumulate in the stomach
(85%), while their proportion in the digestive divertic-
ulum is much lower (3.4%). Heterotrophic bacteria are
mostly localized in the stomach and hindgut (47 and
42%, respectively). While Pseudomonas sp are found
in almost all tissues and organs, Vibrio sp and Acineto-
bacter sp are chiefly isolated from the digestive tract;
these bacteria account for 44% of the bacterial isolate
of the stomach, 68% in the crystalline style, 72% in the
digestive diverticulum, and 81% in the hindgut. The
number of Pseudomonas sp decreases from 27% in the
stomach to 0-3% in the crystalline style and hindgut of
the oyster [56].
In the oyster C. rhizophorae, which is used as a bio-
logical indicator of bacterial contamination of natural
sea waters, heterotrophic bacteria accumulate in the
digestive gland and the posterior intestine; the domi-
nant species are representatives of the Pseudomona-
daceae--solitary bacilliform cells of 0.5-1 x 1.5-4 ~tm
[38]. In M. edulis mussels artificially contaminated
with E. coli, up to 94% of this coliform occurs in the
digestive tract. These microorganisms are found in
much smaller numbers in the gills, muscles, and
haemolymph [68]. Cabelli and Heffernan [35] point out
that V. verrucosa accumulates most of its captured bac-
terial E. coli cells in the siphon tissue and digestive
gland. Studies on the conditionally pathogenic microf-
lora of the scallop Pecten pecten, which were carried
out on oyster farming grounds in four bights in Peter
the Great Bay (Sea of Japan), showed that the highest
number (9 out of 12 species) of bacteria of the genera
Aeromonas, Pseudomonas, Vibrio, and some others
occurs in the hepatopancreas, the organ that accumu-
lates microflora most intensively [1 ].
Thus, most authors conclude that the greater part of
bacteria removed by mollusks from the environment in
the filtration process are finally introduced into the
digestive system.
The subsequent fate of bacterial cells captured by
mollusks is ambiguous: either they are digested in the
digestive system of mollusks, or, not being subject to
lysis and remaining viable, they are agglutinated in the
waste material of the mollusks and thus returned to the
environment. The latter applies to bacteria which, for
one reason or other, do not enter the intestine and are
eliminated from the organism via the pseudofeces
when in contact with the epithelial tissues in the mantle
cavity.
The examples of how bacteria offered as food to
adult and larval bivalves are digested in the bivalve
stomach are many and pertain to various species [33,
69]. In particular, the study of time-courses in the reten-
tion of C 14- and C51-1abeiled bacterial food by the mol-
lusks Potamocorbula amurensis and Macoma baltica
reveals that, in the course of digestion, the feces are
expelled in two portions. The expulsion of the first por-
tion of feces is linked to the completion of the extracel-
lular digestion cycle in the intestine, while the second
is associated with the intracellular digestion of bacteria
in the hepatopancreas. It has been noted that intracellu-
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 26 No. 2 2000
84 GOVORIN
lar digestion of bacterial food is prevalent in P. amuren-
sis, while extracellular digestion is prevalent in M. bal-
tica [41 ].
The role of bacteria in the feeding of mollusks is
dual: bacteria provide an additional source of protein
and aid in the digestion process [69]. Preliminary data
on the "fate" of certain high polymer constituents of
bacterial cells suggest that extracts from the digestive
gland of the mussel M. edulis destroy lysozyme-sensi-
tive microorganisms, and bacteria with lysozyme-sen-
sitive cellular walls rapidly degrade in the mollusk
intestine. On the basis of experimental data, the authors
calculated the ingestion rate of these bacteria, 2 x 108
to 27 x 10 s cells/(ind h). At the same time, lysozyme-
sensitive bacteria such as Micrococcus roseus,
S. aureus, and B. cereus were eliminated from the mus-
sel organism in the intact form [33]. Mention should
also be made of the work of Charles et al. [40] con-
cerned with the filtration of E. coli bacteria by the mol-
lusks V. verrucosa and M. gaUoprovincialis. The
authors constructed mathematical models of filtration
by these mollusks, simulating the distribution of a
radioactive label between the mollusk' s body, dissolved
and particulate organic matter, CO2, feces, and pseud-
ofeces. The assimilation of bacterial cells by the mol-
lusks was fairly low, at 11.1-20.4% for V. verrucosa
and 7.5-14.8% for M. galloprovincialis.
Agglutination of Viable Bacterial Cells
in Mollusk Feces and Pseudofeces
Concomitant with the accumulation of microorgan-
isms in the mollusk' s body and their destruction in the
digestive system, the bacterial cells not subject to lysis
and retaining viability are returned to the environment.
This process can occur in the mollusk gastrointestinal
tract and terminate in the elimination of captured bac-
teria with the feces and through the gill apparatus,
where the retained particles are agglutinated by mucus
and then eliminated via pseudofeces. For example, in
M. mercenaria mollusks artificially contaminated with
E. coli and Salmonella typhimurium bacteria, the latter
are relatively rapidly eliminated within the first 8 h,
after which point the process is retarded. After 24 h, the
density of E. coli declines to a greater degree than that
of S. typhimurium. The bacterial cells are washed out of
the mollusk organism, being attached to the rapidly
deposited fecal and pseudofecal particles with which
these bacteria are usually associated. No ionic bond is
involved in this association [78].
Data on the concentration of viable bacterial cells in
solid waste vary among molluskan species; however,
most investigators agree that these values are insignifi-
cant compared to the degradation rate of microorgan-
isms. Thus, despite the fairly high concentration of bac-
teria in the feces of M. galloprovincialis under experi-
mental conditions (the number of heterotrophic
bacteria is as high as 10 s cells/g and of coliforms,
l 0 s cells/g wet weight), the cumulative concentration
of microorganisms in feces and pseudofeces is not
above 2-3% of their quantity in the volume of water fil-
tered by a mollusk in 1 h. In this event, the contamina-
tion of aggregated waste material was directly propor-
tional to the number of bacteria in the environment
[ 11 ]. In the mollusk V. verrucosa placed in a filtrate of
C~4-1abelled bacterial cultures, 8.8% of the radioactive
label is eliminated with the feces [30].
Mollusk feces and pseudofeces provide a peculiar
substrate for the development of bacteria, protozoans,
and other aquatic organisms. As a consequence, mol-
lusk biodeposits can subsequently affect the content in
sediment of organic matter, including anthropogenic
material, and finally the quality of the marine environ-
ment [19].
It has been experimentally shown that most bacteria
concentrate on the surface of aggregated waste mate-
rial, being adsorbed by the mucous substances of the
envelope. This appears to be true only for the initial
reversible stage of adsorption of microorganisms on the
surface of fecal particles because, during act i ve
mechanical action that can destroy the envelopes, 61 to
77% of the bacterial cells contained in feces may revert
to a suspended state within 24 h of experiment [11].
This process also largely decreases the positive role of
the sedimentation of allochthonic bacteria via aggre-
gated mollusk waste, the microflora of which can sub-
sequently be utilized by detritus feeders dwelling on
the bottom.
The Sanitary and Bacteriological Role of Bivalves
in the Aquatic Environment
Owing to their high filtration capacity, common spe-
cies of bivalves are regarded as biofilters actively par-
ticipating in the transformation of particulate matter in
the coastal zone of the sea. The term "biofilter" was first
proposed by Voskresenskii for M. edulis from the White
Sea [7]. It was suggested that the fouling biocenosis of
coastal water areas be regarded as a belt of filtering
organisms. Later on, Bervald [3] worked out a method
for the biological purification of river waters containing
excessive quantities of organic and mineral particles,
using special tanks in which were placed freshwater
bivalves of the genus Anodonta. He pointed out that
tanks can successfully be replaced by a natural fouling
biocenosis on extra surfaces of various hydrotechnical
constructions. In this regard, we mention a later work
on the role of Anodonta piscinalis in the additional
purification of wastewater from a duck farm in Lietuva
[29]. In all series of the experiment to investigate the
filtration capacity of unionids, the mollusks maintained
their normal physiological state and displayed the abil-
ity to clear the water of both excessive microflora and
particulate organic matter.
In the last decades, the concept of specific use of
bivalves for the additional purification of wastewater
and the biological melioration of the marine environ-
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 26 No. 2 2000
ROLE OF BIVALVES IN THE DEPURATION OF SEAWATERS 85
ment has gained much recognition [21, 25, 42, 46, 57,
74, 79]. In a number of countries, these scientific devel-
opments have been applied in practice [58, 59]. In so
doing, there is a tendency for the use of treated and
untreated wastewater in agriculture and aquaculture to
increase in both developed and developing countries
[48]. A large body of publications is generally con-
cerned with the problems of utilization of mollusks for
the purification of the aquatic environment containing
excessive quantities of organic material, mineral parti-
cles [2, 16, 18, 19, 57, 71], and heavy metals [23, 25].
At the same time, there are still fairly few studies of the
various aspects of the use of filtering mollusks to lessen
the bacterial contamination of inshore sea areas.
In Russian-language literature concerned with the
problems of sanitary bioamelioration of the marine
environment, the role of the mussels M. edulis and
M. galloprovincialis has been extensively explored;
however, the use of other common species of bivalves
for these purposes has been poorly investigated. The
high potential of M. galloprovincialis mussels culti-
vated on collectors for the enhancement of the marine
environment in the coastal area near Odessa has been
reported. Despite the fact that the area of observation
was continuously contaminated by heavy discharges of
domestic sewage, the passage of waters through a num-
ber of units of the "Rif" mussel mariculture installation
reduced the bacterial contamination (p < 0.05) in 76%
of the cases. With a fairly high level of seawater con-
tamination by heterotrophic microorganisms (10 -s-
10 7 cells/liter) and coliforms (102-104 cells/liter), the
maximal positive effect of bioamelioration was as great
as 87 and 92%, respectively, with average values for
many years of observations being 43-52% [13]. The
removal efficiency of bacteria at the middle depth hori-
zon (5 m) was consistently higher than in the near-bot-
tom layer (9 m); the numbers of bacteria in the water
decreased, on the average, by 52.3 and 33.7% for het-
erotrophic microorganisms and by 65.1 and 44.0% for
coliform bacteria, respectively. These discrepancies
were primarily due to depth-related differences in the
number and biomass of mussels on collectors; up to
47% of the overall biomass occurred in the upper por-
tion of the mariculture unit and only 18.5% in the near-
bottom part. The clearance capacity of "Ri f ' was
inversely related to the contamination of the environ-
ment and bacterial pressure on the mollusks. Usually,
hardly any effect is found (10.3% of cases) with low
flow velocity and slow water motion, which are charac-
teristic of 9- to 10-m depths. It is not possible to state
with full assurance that the bioamelioration effect is
equal to 0, because mollusks can repeatedly filter a
small volume of water immediately adjacent to them.
The clearance efficiency may even increase, but the
volume of water in the depuration layer will remain
limited.
The ability of bivalves to accumulate various micro-
flora in their organs can be a real hazard to potential
consumers since mollusks, actively participating in the
purification of the marine environment, are frequently
carriers of pathogenic microorganisms and viruses.
Eating raw mollusks is often the cause of food poison-
ings, allergies, and infectious diseases [75]. Therefore,
mollusk mariculture for the sanitary bioamelioration of
coastal areas is limited because of the problems of sub-
sequent utilization of heavily contaminated mollusks.
The existing routine techniques were devised for the
depuration of modestly contaminated mollusks and
involve their maintenance in special tanks or pools with
circulating seawater previously disinfected by ultravio-
let radiation or ozone over a brief depuration cycle [49,
72, 78]. As a rule, it is hardly possible to purify M. gal-
loprovincialis that contains E. coli concentrations in
excess of 102 cells/g in the tissue over 18-24 h [9]. In
environmentally contaminated C. virginica and
M. mercenaria mollusks, the numbers of fecal E. coli
and Salmonella sp coliforms declined to an undetect-
able level within 14 days [54]. Clearly, this depuration
time is inappropriate for large-scale purification.
The results of observations on large-scale depura-
tion of the mollusks M. mercenaria indicate that depu-
ration efficiency is entirely dependent on the level of
contamination of mollusks, and that their full depura-
tion over 24 h can occur only at an initial concentration
of E. coli not above 102-103 cells/100 g soft tissue
homogenate. In case the initial contamination of mol-
lusks is greater than 105 cells/100 g, only 40% of the
mollusks are decontaminated within a 48-h depuration
period [49]. More efficient methods, such as oxygen
hydrolysis or high temperature drying, should probably
be used with heavily contaminated mollusks for the
safe elimination of pathogenic microflora. The hydro-
lyzates can be utilized in the pharmaceutical industry
and for the production of various medicines, while the
flour provides a valuable food supplement for livestock.
The use of common species of bivalves for improv-
ing the sanitary and bacteriological characteristics of
the sea requires entirely novel types of mariculture col-
lectors to be devised. These systems must differ accord-
ing to the function to be fulfilled: the elimination of
allochthonic bacteria in zones of continuous discharge
of domestic and industrial sewage or the additional
depuration of recreation zones of the sea [6]. To resolve
the problem of efficient use of mollusks for the bioame-
lioration of inshore areas of the sea and for increasing
the purification potential of the marine environment,
extensive studies in sea areas with different bacterial
pressure are needed.
.
REFERENCES
Avdeeva, N.V. and Filipchuk, E.S., Conditionally Patho-
genic Microflora of Scallops on Scallop Farming
Grounds in Peter the Great Bay, Vsesoyuznaya konferen-
tsiva po morskoi biologii, Sevastopol', Okt. 1988: Tezisy
dokladov (Abstracts of Papers, All-Union Conf. on
Marine Biology, Sevastopol, Oct. 1988), Kiev, 1988,
part 2, p. 47.
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 26 No. 2 2000
86 GOVORIN
32. Alemov, S.V., Creation of Artificial Mussel Populations
for Hydrobiological Purification of Oil-containing Sea
Waters, Iskusstvennye rify dlya rybnogo khozyaistva,
Tezisy dokladov Vsesoyuznoi konferentsii (Artificial
Reefs for Fisheries, Abstracts of Papers, All-Union
Conf.), Moscow: Vsesoyuz. Nauch.-Issled. Inst. Ryb.
Khoz. Okeanogr., 1987, pp. 69-71.
3. Bervald, E.A., Biological Purification of Waters Using
Filtering Tanks, Materialy l s" ezda Vsesoyuznogo gidro-
biologicheskogo obshchestva (Proc. I Congress of All-
Union Hydrobiological Society, 1965), Moscow: Nauka,
1965, pp. 31-32.
4. Bonev, S. and Zakhariev, Z., Epidemiol., Mikrobiol.
lnfekts. Bolesti, 1972, vol. 9, no. 1, pp. 42--47.
5. Valyavskaya, G.I. and Rybak, A.A., Current Ecological
and Hygienic Problems of Pollution of the Seas, Ekolo-
gicheskoe sostoyanie rekreatsionnoi zony yuga
evropeiskoi chasti SSSR, Tezisy dokladov Vsesoyuznoi
konferentsii (Ecological Situation in the Recreation
Zone in the Southern European Part of the USSR,
Abstracts of Papers, All-Union Conf.), Tbilisi, 1990,
pp. 77-78.
6. Vityuk, A.V., Gubanov, V.V., and Zaitsev, Yu.P., "Ri f'
System for Commercial Cultivation of Mussels and
Improvement of the Marine Environment, Iskusstvennye
rify dlya rybnogo khozyaistva, Tezisy dokladov Vse-
soyuznoi konferentsii (Artificial Reefs for Fisheries,
Abstracts of Papers, All-Union Conf.), Moscow: Vse-
soyuz. Nauch.-Issled. Inst. Ryb. Khoz. Okeanogr., 1987,
pp. 69-71.
7. Voskresenskii, K.A., Belt of Filtering Organisms as a
Biological System of the Sea, Tr. GOIN, 1948, voi. 6,
no. 18, pp. 55-119.
8. Gerlakh, S.A., Zagryaznenie morei: Diagnoz i terapiya
(Pollution of the Seas: Diagnosis and Therapy), Lenin-
grad: Gidrometeoizdat, 1985.
9. Govorin, I.A., Samoochishchenie chernomorskoi midii
Mytilus galloprovincialis Lain. ot bakterial'nogo
zagryazneniya i faktory, opredelyayushchie ego effek-
tivnost" (Depuration of the Black Sea Mussel Mytilus
galloprovincialis Lam. Contaminated by Bacteria and
Factors Determining Its Efficiency), Available from
VINITI, 1987, Odessa, no. 377-B87.
10. Govorin, I.A., Role of Black Sea Mussels in the Elimi-
nation of Allochthonic Bacteria from the Marine Envi-
ronment, Gidrobiol. Zh., 1991, vol. 27, no. 4, pp. 33-38.
11. Govorin, I.A., Sanitary and Bacteriological Importance
of the Aggregated Waste Material of Black Sea Mussels,
Biol. Morya, 1993, no. 1, pp. 98-111.
12. Govorin, I.A. and Adobovskii, V.V., Effect of Underwater
Discharge of Municipal Sewage on the Bacteriological
Characteristics of Coastal Waters in the Northwestern
Black Sea, Gigiena i Sanitariya, 1992, no. 2, pp. 20-22.
13. Govorin, I.A., Adobovskii, V.V., and Katkov, V.N., Sani-
tary and Bacteriological Aspects of Mussel Mariculture
for Bioamelioration of the Marine Environment, Gidro-
biol. Zh., 1994, vol. 30, no. 1, pp. 44-53.
14. Bergey's Concise Manual. Translated under the title
Kratkii opredelitel' Bergi, Moscow: Mir, 1980.
15. Kurenkov, I.I., Red Tide in Avachinskaya Bay, Ryb.
Kho~, 1974, no. 4, pp. 20-21.
16. Milovidova, N.Yu. and Kiryukhina, L.N., Chernomor-
skii makrozoobentos v sanitarno-biologicheskom aspe-
kte (Macrozoobenthos of the Black Sea in the Biosani-
tary Aspect), Kiev: Naukova Dumka, 1985.
17. Mironov, G.N., Filtering Activity and Feeding of Mus-
sels of the Black Sea, Tr. Sevastop. Biol. Stn., 1948,
vol. VI, pp. 338-352.
18. Mironov, O.G., On the Use of Aquatic Organisms in
Marine Pollution Control, Gidrobiol. Zh., 1985, vol. 21,
no. 5, pp. 24-28.
19. Mironov, O.G., Mussels as a Component of the Hydro-
biological System of Purification of Polluted Marine
Waters, Vod. Resursy, 1988, no. 5, pp. 104-111.
20. Nizhegorodova, L.E. and Nidzvetskaya, L.M., Bacterial
Flora of Mussels of the Bay of Odessa, Gidrobiol. Zh.,
1980, vol. 16, no. 1, pp. 85-89.
21. Nizhegorodova, L.E. and Nidzvetskaya, L.M., Effect of
Reefs of Different Design on the Microflora and Bacte-
rial Processes in Seawater (Odessa Coast), Iskusstvennye
rify dlya rybnogo khozyaistva, Tezisy dokladov Vse-
soyuznoi konferentsii (Artificial Reefs for Fisheries,
Abstracts of Papers, All-Union Conf.), Moscow: Vse-
soyuz. Nauch.-Issled. Inst. Ryb. Khoz. Okeanogr., 1987,
pp. 37-39.
22. Nizhegorodova, L.E. and Nidzvetskaya, L.M., Effect of
the Dunai River Runoff on the Microbiocenosis of the
Northwestern Black Sea, Tezi sy dokladov !II Vse-
soyuznoi konferentsii po morskoi biologii (Abstracts of
Papers, III All-Union Conf. on Marine Biology), Kiev,
1988, part 2, pp. 126-127.
23. Pavlova, E.S., Mollusks as Indicators of Migration and
Distribution of Metals in Shelf Ecosystems, Dokl. MOIP,
Zool. Bot., Moscow: Mosk. Gos. Univ., 1987, pp. 24-26.
24. Puchenkova, S.G., Sanitary and Microbiological Assess-
ment of Seafoods, Metody obnaruzheniya indikatornoi,
patogennoi i potentsial'no patogennoi mikroflory v
ob"ektakh okruzhayushchei sredy v svyazi s vliyaniem
antropogennykhfaktorov (Methods for the Identification
of Indicatory, Pathogenic, and Potentially Pathogenic
Microflora in the Environment in Connection with
Anthropogenic Impact), Moscow, 1987, pp. 99-104.
25. Saenko, G.N., Role of Mariculture in Biosphere Protec-
tion, Tezisy dokladov Mezhdunarodnogo simpoziuma po
sovremennym problemam marikul'tury v sotsialis-
ticheskikh stranakh (Abstracts of Papers, International
Symp. on Current Problems of Mariculture in Socialist
Countries), Moscow, 1989, pp. 17-18.
26. Sorokin, Yu.I., Bacteria as Food for Coral Reef Fauna,
Okeanologiya, 1972, vol. 12, no. 2, pp. 195-204.
27. Sorokin, Yu.I., Petipa, T.S., and Pavlova, E.V., Quantita-
tive Study of the Nutritive Role of Bacterioplankton,
Okeanologiya, 1970, vol. 10, no. 2, pp. 332-340.
28. Tkacheva, R.I., Stroeva, M.N., Serenko, V.I., et al.,
Dynamics of the Sanitary Status of Riverine and Marine
Water in the Southern Zone of the Russian Soviet Fed-
eral Socialist Republic, Ekologicheskoe sostoyanie
rekreatsionnoi zony yuga evropeiskoi chasti SSSR, Tezisy
dokladov Vsesoyuznoi konferentsii (Ecological Situation
in the Recreation Zone of the Southern European Part of
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 26 No. 2 2000
ROLE OF BIVALVES IN THE DEPURATION OF SEAWATERS 87
the USSR, Abstracts of Papers, All-Union Conf.),
Tbilisi, 1990, pp. 83-84.
29. Shivokene, Ya., Shal'chute, B., and Sinyavichene, D.,
Use of Bivalve Mollusks for Additional Treatment of
Wastewater from Duck Farms, Biologicheskie resursy
vodoemov basseina Baltiiskogo morya, Materialy XXI !
nauchnoi konferentsii po izucheniyu vodoemov Pribal-
tiki (Biological Resources of Water Bodies of the Baltic
Sea Region, Proceedings of XXII Conf. on Water Bodies
of the Baltic Sea Region), Vilnius, 1987, p. 219.
30. Amouroux, J.-M., Preliminary Study on the Consump-
tion of the Dissolved Organic Matter (Exudates) of Bac-
teria and Phytoplankton by Marine Bivalve Venus verru-
cosa, Mar. Biol., 1984, vol. 82, no. 2, pp. 109-112.
31. Aubert, M., l~tude des modalit6s de contamination
bact6rienne des moules: essai de mise au point d'un test
repr6sentatif de 1'6tat sanitaire de I'eau de mer littorale,
Oceanus, 1988, vol. 14, no. 1, pp. 109-112.
32. Bernard, ER., Uptake and Elimination of Coliform Bac-
teria by Four Marine Bivalve Mollusks, Can. J. Fish.
Aquat. Sci., 1989, no. 46, pp. 1592-1599.
33. Birkbeck, T.H. and McHenry, I.G., Degradation of Bac-
teria by Mytilus edulis, Mar. Biol., 1982, vol. 72, no. I,
pp. 7-15.
34. Blake, P.A., Rosenberg, M.L., Bandeira, C.J., et al.,
Cholera in Portugal, 1974. I. Modes of Transmission,
Am. Epidemiol., 1977, vol. 105, no. 4, pp. 337-343.
35. Cabelli, V.J. and Heffernan, W.P., Accumulation of
Escherichia coli by the Northern Quahaug, Appl. Micro-
biol., 1970, vol. 19, no. 2, pp. 239-244.
36. Castelli, J., Flora bacteriana marina, acumulada por ill-
tracion en Mytilus edulis, Invest. Pesq., 1966, no. 30,
pp. 639-65 i.
37. Castro, A., Gonzalez, J., Espeleta, C., and Carrera, J.,
Presencia de Salmonella en ostiones, Cuba, 1985-1988,
Rev. Cub. Hig. Epidemiol., ! 990, vol. 28, no. 1, pp. 88-93.
38. Cerutti, R.L. and Barbosa, T.C.P., Flora bacteriana het-
erotrofica em ostras (Crassostrea rhizophorae) e aguas
da baia Norte, ilha de Santa-Catarina, Brasil, Rev. Micro-
biol., 1991, vol. 22, no. 4, pp. 330-334.
39. Charles, E, Gremare, A., Amouroux, J.-M., and Ca-
chet, G., Filtration of the Enteric Bacteria Escherichia
coli by Two Filter-Feeding Bivalves, Venus verrucosa
and Mytilus galloprovhtcialis. I. Experimental Study,
Mar. Biol., 1992, vol. 113, no. I, pp. 117-124.
40. Charles, E, Amouroux, J.-M., Gremare, A., and Cachet, G.,
Filtration of the Enteric Bacteria Escherichia coli by
Two Filter-Feeding Bivalves, Venus verrucosa and Myti-
lus galloprovincialis. II. Modelling, Mar. Biol., 1992,
vol. 113, no. I, pp. 125-131.
41. Decho, A.W. and Luoma, S.N., Time-Courses in the
Retention of Food Material in the Bivalves Potamocor-
bula amurensis and Macoma baltica: Significance to the
Adsorption of Carbon and Chromium, Mar. Ecol. Prog.
Ser., 1991, vol. 78, no. 3, pp. 303-314.
42. Devik, E.O., Hat vest i ng Pol l ut ed Waters. Waste Heat
a l ~ Nutrient-loaded Effluents in the Aquaculture, New
York: Plenum Press, 1976, XII.
43. Dutt, A.K., Syea, A., and Velauthan, T., A Shellfish-
borne Cholera Outbreak in Malaysia, Trans. Roy. Soc.
Trop. Med. Hyg., 1971, vol. 65, no. 6, pp. 815-818.
44. Galtsoff, ES., The Effect of Temperature on the Mechan-
ical Activity of the Gills of the Oyster (Ostrea virginica
Gmelin), J. Gen. Physiol., 1928, no. I l, pp. 415-431.
45. Gauthier, M.J. and Brittymayer, V.A., La pollution
bact6rienne de lamer, Recherche, 1990, vol. 21, no. 223,
pp. 910-912.
46. Gomoiu, M.-T., Potential Role and Ecological Effects of
Artificial Reefs Constructed on the Coastal Sandy Bot-
tom of the Black Sea (Romania), Trav. Mus. Hist. Natur.
"Gr. Ant i pa, " 1989, vol. 39, no. 30, pp. 291-306.
47. Haven, D.S. and Morales-Alamo, R., Filtration of Parti-
cles from Suspension by the American Oyster Crassos-
trea virginica, Biol. Bull., 1970, no. 139, pp. 246-264.
48. Health Guidelines for the Use of Wastewater in Agricul-
ture and Aquaculture, Techn. Report Ser. WHO, 1989,
no. 778.
49. Heffernan, W.E and Cabelli, V.J., The Elimination of Bac-
teria by the Northern Quahaug: Variability in the Response
of Individual Animals and the Development of Criteria,
Proc. Nat. Shellfish Ass., 1971, no. 61, pp. 102-108.
50. J/Srgensen, C.B., The Rate of Feeding by Mytilus edulis
in Different Kinds of Suspension, J. Mar. Biol. Ass. U.K.,
1949, no. 28, pp. 333-344.
51. J6rgensen, C.B., Efficiency of Particle Retention and
Rate of Water Transport in Undisturbed Lamellibranchs,
J. Cons. hzt. Explor. Mer., 1960, no. 26, pp. 94--116.
52. J~rgensen, C.B., Famme, P., Kristensen, H.S., et al., The
Bivalve Pump, Mar. Ecol. Prog. Ser., 1986, no. 34,
pp. 69-77.
53. J6rgensen, C.B., Larsen, P.S., Mohlenberg, F., and Riis-
gard, H.U., The Mussel Pump: Properties and Model-
ling, Mar. Ecol. Prog. Ser., 1988, no. 45, pp. 205-216.
54. Kator, H. and Rhodes, M., Microbiological Evaluation
of Relaying for Purification of Contaminated Shellfish,
87th Annual Meet i ng o f the Am. Soc. Microbiol., Atlanta,
1-6 March, 1987, Washington, D.C., 1987, p. 301.
55. Kemp, P.F., Neweil, S.Y., and Krambeck, C., Effect of
Filter-Feeding by the Ribbed Mussel Geukensia demissa
on the Water- Column Microbiota of a Spartina alterni-
f l ora Saltmarsh, Mar. Ecol. Prog. Ser. , 1990, vol. 59,
nos. 1-2, pp. 119-131.
56. Kueh, C.S.W. and Chan, K.-Y., Bacteria in Bivalve
Shellfish with Special Reference to the Oyster, J. Appl.
Bacteriol., 1985, no. 59, pp. 41--47.
57. Larsson, A.-M., Blue Mussel Sea Farming--Effects on
Water Quality, Vatten, 1985, voi. 41, no. 4, pp. 218-224.
58. Mann, R. and Taylor, R.E., Jr., Public Health Aspects of
the Culture of the Japanese Oyster Crassostrea gigas in
a Waste Recycling Aquaculture System, Aquaculture,
1983, vol. 30, nos. 1--4, pp. 311-327.
59. Martin, Y., Bonnefont, J.L., and Guinnet, B., Risques
sanitaires li6s a I'utilisation des effluents urbains en
aquaculture marine, Techn., Sci., Meth., 1990, no. 9,
pp. 413--420.
60. Mason, J.O. and MacLean, W.R., Infectious Hepatitis
Traced to the Consumption of Raw Oysters, Am. J. Hyg.,
1962, pp. 90-111.
61. McHenry, J.G. and Birkbeck, T.H., Uptake and Process-
ing of Cultured Microorganisms by Bivalves, J. Exp.
Mar. Biol. Ecol., 1985, vol. 90, no. 2, pp. 145-163.
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 26 No. 2 2000
88 GOVORIN
62. Metcaif, T. and Stiles, W., The Accumulation of the
Enteric Viruses by the Oyster Crassostrea virginica,
J. Infect. Dis., 1965, no. 115, pp. 68-76.
63. Meyer-Rochow, V.B., Observations on an Accidental
Case of Raw Sewage Pollution in Antarctica, Zbl. Hyg.
Umweltmed., 1992, vol. 192, no. 6, pp. 554-558.
64. Minet, J., Barbosa, T., Prieur, D., and Cormier, M., Mise
en 6vidence du processus de concentration des bact6ries
par la moule Mytilus edulis, C. R. Acad. Sci. (Paris),
Ser. III, 1987, vol. 305, pp. 351-354.
65. MOhlenberg, E and Riisgard, H.U., Efficiency of Particle
Retention in 13 Species of Suspension Feeding Bivalves,
Ophelia, 1978, no. 17, pp. 239-246.
66. Olaczyk-Neyman, K., Mikrobiologiczne aspekty zaniec-
zyszczenia w6d morskich ciekami, lnz. Mor., 1980,
vol. 1, no. 11, pp. 390-391, 393-395.
67. Owen, G., Feeding and Digestion in the Bivalvia, Adv.
Comp. Physiol. Biochem., 1974, vol. 5, pp. 1-35.
68. Power, U.E and Collins, J.K., Tissue Distribution of a
Coliphage and Escherichia coli in Mussels after Con-
tamination and Depuration, Appl. Environ. Microbiol.,
1990, vol. 56, no. 3, pp. 803-807.
69. Prieur, D., Nouvelles donn6s sur relations entre bact6des
et bivalves marins, Haliotis, 1981, no. 11, pp. 251-260.
70. Prieur, D., Mevel, G., Nicolas, J.-L., et al., Interactions
between Bivalve Mollusks and Bacteria in the Marine
Environment, Oceanogr. Mar. Biol. Annu. Rev., 1990,
no. 28, pp. 277-352.
71. Rodhouse, P.G. and Roden, C.M., Carbon Budget for a
Coastal Inlet in Relation to Intensive Cultivation of Sus-
pension-feeding Bivalve Mollusks, Mar. Ecol. Prog.
Ser., 1987, vol. 36, no. 3, pp. 225-236.
72. Rodrick, G.E., Schneider, K.R., Steslow, E, and Bla-
cke, N.J., Uptake, Fate and Elimination by Shellfish in a
Laboratory Depuration System, Oceans' 87 Proceed-
ings, Ocean-Int. Workplace, 1987, New York, 1987,
vol. 5, pp. 1752-1756.
73. Spittler, P., de la Alfredo, C.S., Rodriquez, J., La selec-
cion del tama6 de las particulas alimenticias por el osti6n
Crassostrea rhizophorae, Re v . Invest. Mar., 1989,
vol. 10, no. 1, pp. 63-70.
74. Stirn, J., Pokleka, D., and Vukovic, A., Ciscenje komu-
nalnih voda z reciklazo v marikulturah, Hem. Ind., 1977,
vol. 31, no. 7, pp. 357-360.
75. St6ven, K., Krank durch Muschelgenu, Lebensmit-
teltechnik, 1980, vol. 12, no. 1 I, pp. 26-29.
76. Takase, A. and Bito, T., The Utilisation of Radioisotope
Labelled Bacteria in the Food Sanitation Studies. III. On
the Bacterial Contamination of Living Oysters, Preprint
of the 4th Japan Conf. Radioisotopes (JRIA), 1961.
77. Tammes, P.M.L. and Dral, A.D.G., Observations on the
Straiting of Suspensions by Mussels, Arch. Ned. Zool.,
1955, vol. 11, pp. 87-111.
78. Timoney, J.E and Abston, A., Accumulation and Elimi-
nation of Escherichia coli and Salmonella typhimurium
by Hard Clams in an "In Vitro" System, Appl. Environ.
Microbiol., 1984, vol. 47, no. 5, pp. 986-988.
79. Utilisation of Sewage Effluent for Shellfish Culture, FAO
Aquacult. Bull., 1972, vol. 5, no. 1, p. 4.
80. deVilliers, C.J. and Allanson, B.R., Efficiency of Particle
Retention in Solen cylindraceus (Hanley) (Mollusca:
Bivalvia), Estuar. Coast. Shel f Sci . , 1988, vol. 28, no. 4,
pp. 421-428.
81. Wright, R.T., Coffin, R.B., Ersing, C.P., and Pearson, D.,
Field and Laboratory Measurement of Bivalve Filtration
of Natural Marine Bacterioplankton, Limnol. Oceanogr.,
1982, vol. 27, no. 1, pp. 91-98.
82. ZoBell, C.E. and Feltham, C.B., Bacteria as Food for
Certain Marine Invertebrates, J. Mar. Res., 1937, no. 1,
pp. 312-327.
RUSSIAN JOURNAL OF MARINE BIOLOGY Vol. 26 No. 2 2000

You might also like