Role of Bivalves in the Depuration of Seawaters.pdf

8/11/2019 Role of Bivalves in the Depuration of Seawaters.pdf

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Rus,~ian Journal o f 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

R o l e o f i v a lv e s in t h e D e p u r a t i o n o f S e a w a t e r sC o n t a m i n a t e d b y a c t er ia

I A G o v o r i n

Odessa Branch Institute of the Biology of Southern Seas National Academ y o f Sciences of the U krainOdessa 270011 UkraineRece ived Janu ary 11, 1999

Ab stract--B acte r ial contaminat ion the inshore areas o f seas, is current ly one of the most comm on mantions of increasing anthropogenic pressure on aquatic ecosystems. Permanent sources of allochthonic mlora in the inshore areas o f seas, are p olluted w ith untreated or insufficiently treated dom estic and indsew age [5, 8, 12, 45, 66] an d river run-off from areas of active w ater use [22, 28], and suffer the effects oexploitation of beaches during the bathing se ason (in the summ er).

I n r ecen t yea r s , h i gh l eve l s o f bac t e ri a l con t am i na -

t i on o f m ar i ne wa t e r s have been de t ec t ed i n va r i ousr eg i ons o f t he wor l d , i nc l ud i ng t hose p r ev i ous l yt hough t t o be eco l og i ca l l y s a f e [ 63 ].

Unde r t he se cond i t i ons , i t ha s becom e i nc r ea s i ng l yimpor tant to s tudy the na tura l pur i f i ca t ion of sea watersand t he s an i t a r y r o l e o f s e l ec t ed spec i e s o f aqua t i co rgan i sm s , pa r t i cu l a r l y b i va l ves , wh i ch a r e am ong t hem os t a c t i ve f i lt e r ing o rgan i sm s . Bec ause o f t he i r unsa t -i s f ac t o r y s an i t a r y and hyg i en i c cha r ac t e r i s t i c s , m anyi nshor e a r ea s o f t he s ea s a r e becom i ng unsu i t ab l e f o rm ol l u sk m ar i cu l t u r e . Cons i de r i ng t he s t eady l o s s o fecosys t em s wi t h l ow bac t e r i a l p r e s su r e , t he cu r r en ts t ra t egy o f b i va l ve m ar i cu l t u r e ne eds t o be chang ed . I npa r t icu l a r, com m on spec i e s o f m o l l u sks a r e po t en t i a l lyve r y use f u l i n t he b i oam e l i o r a t i on o f t he m ar i ne env i -r onm en t [ 48 ] . Howeve r, t he s an i t a r y and bac t e r i o l og i -c a l r o l e o f m a r i c u lt u r e f ar m s m u s t b e c o m p r e h e n s i v e l yand t ho r ough l y s t ud i ed .

I n t h is r ev i ew, a t ten t i on i s f ocused on t he m i c r ob i o -l og i ca l a spec t s o f t he i n t e r ac t i ons o f b i va l ve m o l l u sksa n d t h e e n v i r o n m e n t .

Eff ic i en cy o f Re ten tio n an d A ccu mu la t io no f Micro o rg an isms b y Mo l lu sk s

The h i gh f i lt r at ion capac i t y o f b iva l ves was de m o n-s t ra t ed a s ea r l y a s t he 1920- 194 0s by a num ber o finves t iga tors [7 , 17 , 44 , 50] . The re a re a var ie ty of opin-ions as to the par t i c le se lec t iv i ty and f i l tra t ion e ff i c iencyo f m o l lu s k s . J r r g e n s e n [ 5 0 - 5 3 ] s h o w e d t h at s o m eb i va l ves e f f i c i en t l y r e t a i n pa r t i c l e s o f a f ew m i c r ons .Haven and Mor a l e s - Al am o [ 47 ] f ound t ha t t he oys t e rCrassostrea virghlicare ta ins 1-3 l am par t i c les wel l ,a l thou gh the f i l t r a tion e ff i c iency i s l ess than 100% .

Spi t t l e ret al. [ 73 ] showed t ha t t he oys t e rC. rhizo-p h o rae r e t a i n s f ood pa r t i c le s o f a wi de s i ze r ange , p r e -fe r r ing par t i c les f rom 25 to 56 l am, a l though i t a l so

i nges t s ve r y sm a l l pa r t i c l e s o f l e s s t han 1 l i m i n d i

t e r. The m o l l u skSolen cy l indraceusr e ta i n s 7 0 - 9 0 % o fses ton pa r t i c les of 2 .5 -3 ~tm; be lo w the s ize of 2 pmf i l t r a t i on e f f i c i ency i s m ar ked l y r educed [ 80 ] . I n c l a s s i c w or k on t he f i lt r at i on o f va r ious suspens i ont he m usse lMyti lus edu l i sTam m es and Dr a l [ 77 ]em phas i z e t ha t r e t en t ion e f f i c i ency i s p r i m ar i l y r eto par t i c le s i ze . In l ine wi th th i s observa t ion , au thors id ent i fy a s i ze group of par t i c les (7-8 lxm)a r e f u l ly r e t a i ned by t he m o l l u sk and a g r oup o f smpa r t ic l e s t ha t t he m u sse l i s unab l e t o r e t a i n du r i ngpr opu l s i on o f wa t e r t h r ough i t s g i l l appa r a t us (2 .5 l .tm f rage l la tes and bac te r ia ) .

Thus , a num ber o f au t ho r s have po i n t ed ou t m o l l u sks can cap t u r e pa r t i c l e s l a rge r t han 2 - 3 l amwe l l a s pa r t i c l e s o f I - 3 / am and sm a l l e r [ 64 , 65 , Th i s pa r t i c le s i z e r ange m a t ches t he ce l l d im en s i ova r i ous au t och t honous m ar i ne m i c r oo rgan i sm s col i form bac ter ia , which a re universa l indica toranthro poge nic po l lu t ion of the aqua t ic envi ron me nt

Da t a on t he r e t en t i on e f f i c iency o f va r i ous m i c rg a n i s m s b y b i v a l v e s a r e a m b i g u o u s a n d s o m e tcon t r ove r s i a l . On t he one hand , t he occu r r enc

d i ve r se a l i och t hon i c m i c r o f l o r a i n m o l l u sks , i nc l ui nd i ca t o r y and pa t ho gen i c en t e r i c bac t e r i a such a sBac-ter ium co li Salmo nel laa n d Shigel la sp, Vibrio chol-erae and V. parah aem oly t icushas been we l l docu -m en t ed f o r con t am i na t ed s ea a r ea s [ 4 , 20 , 24 , 3662] . I n a nu m b er o f coun t r i e s , e a t i ng r aw o r i n sc i en t l y the r m a l l y p r oces sed m ol l u sks ha s been r epto cause she l l f i sh poi soning [15 , 34 , 43 , 60] . Ono t he r hand , t he m echan i sm o f r e t en t i on o f bac t e rb iva lves , i ts e ffi c iency, and pr im ar i ly the fur the r facap t u r ed bac t e r i a l c e l ls r em a i ns t o be s t ud i ed .

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Efficiency o f Rem oval by Mollusks o f Microbial C ellsfrom Bacterial Suspension

A number of au thors have noted the low percentre tent ion by mol lusks of so l i t a ry bac te r ia l ce l l s f romsuspens ion . The oys te rOstrea virginicai s only able toretain a smal l par t of the bacter iaB. coli(1 .1-1 .5 x 2 .0-6 .0 ~ tm) adde d to nat ive seawater, wh i le 70-9 0 of thebac ter ia avoid pass ing through the g i l l s , and can be

found only in water f i lt e red out by m ol lusk [44] . There tent ion e ff i c iency of bac te r ia by the m usse lM. edulisin exper im ents us ing m icrobia l ce l ls of 0 .5-2 .5 ~ tm wasin the range f rom 5 to 24 [77]. How ever, the authorsremark tha t the resul t s a re based on only t en observa-t ions per fo rmed w i th a l imi ted num ber of an imals .

As ear ly as the 1930s, i t was noted that musselsact ively set tle out suspen sions o f bacter ial cel ls and canl ive for a long t ime w i thout any o ther food [82].

McHenr y and Bi r kbeck [ 6 l ] dem ons t r a t ed t ha tM. eduIis, O. edulis, and Mya arenariacapture evensol it a ry bac te r ia l ce l l s f rom suspens ion , wh i le the mo l -lusk Chlamys operculariscan only do so f rom the a lgo-bac ter ia l mixture ofEscherichia coli and Tetraselmissuecica. Theaddi t ion of the l a t t er to cu l tured microor-ganisms enhan ces the f i lt r at ion ra tes byM. edulis andO. edulis.I t i s the rate bu t no t the eff iciency of f i l t rationthat increases, s inceE. coli cel ls do at tach to the algae.

For many b iva lves such asCardium echinatum,Mo diolus m odiolus, and Arctica islandica,part icles ofup to 1 lam are not l imi t ing . H owever, mos t au tochtho-no us bac ter ia are less than 1 lam in diameter ; therefore,the c learance e ff i c iency of these bac te r ia i s not abo ve20-3 0 . Never the less , som e mol lusks , such asGeu-kensia demissa,are able to re ta in bac te r ia of 0 .2-0 .4

and 0.4--0.6 ktm with an eff iciency of 30 and 86 ,respec tive ly. The remov al e ff i c iency of cyan obac ter iaand so me o ther bac te r ia by these mo l lusks var ies f rom25 to 56 per hour. I t has a lso been noted tha t bac te r iaare not re ta ined , as wel l as medium-s ized l iv ing phy-toplankton organ isms o r f l akes of organic mater ia l (upto 95 ) , a l though the removal e ff ic iency of par t ic les i snot de pen den t solely on par t icle s ize [55].

Labora tory measurements of f i l t r a t ion of na tura lmar ine bac te r ioplankton by the mol lusksM. edulisandM. arenaria indicate that bacter ia of m ore than 0.5 lamin size are removed more eff icient ly [81] . In experi -ments , the mol luskVenus verrucosaassimilates about

1460 of C - l abe l ledLactobacillus sp. added to nat iveseawater. The h ighes t amoun t of C14was fou nd in thevi scera l ti s sue , g i l l s, and mant le wh en exp ressed basedon d ry w eigh t in the gi l ls [31] .

The B l ack Sea m usse lMytilus gaUoprovincialiswasfound to remo ve a l a rge quant i ty o f a l lochthonic bac te -r i a f rom na t ive seawater exper imenta l ly contamina tedby domest ic sewage [10] . At opt imal t empera ture andsal ini ty (18~ and 15 to 16 0) and active wate r mo tion,the remov al ra te of bac te r ia f rom suspens ion was 6 .4 x104-2 .0 x 107 ce l ls / ( ind h) for 1 7-18 m m m usse l s and7.6 x 105-1.6 x l0 s ce l l s /( ind h) for 55-6 0 m m m usse l s .

Mu sse l s e l imina ted 54 .5-71 .0 of the he te ro trophbac ter ia and 68 .0-76 .0 of the enter ic bac te r ia f rothe water mixture . The average va lues of e l imina t iow e r e 3 8 . I - 5 9 . 6 f o r I 7 - 1 8 m m m u ss e ls a n d 4 9 . 963.6 for 55--60 m m musse l s .

I t should be n oted that , for f i lter-feeding organ ismsuch as b iva lves , a long w i th the concent ra t ion o f bac tr i a l ce ll s , the degree o f the i r aggrega t ion i s imp or tant

the re tent ion of microorganisms captured f rom thenvi ronment . Sorokinet al. [26, 27] showed that 30 to40 of na tura l bac te r ioplankton ce ll s a re uni ted inaggrega tes of mo re than 4 k tm in s ize and, be ing aggrgated, are easi ly captured even by coarse f i l ter inorganisms such as musse l s and oys te rs .

Exper imenta l s tudies have demons t ra ted tha t thadsorpt ion of bacter ial cel ls is direct ly related to m olusk spec ies and envi ronm enta l tempera ture . Alm ost au thors poin t out tha t seawater t empera ture l a rgeaffects the physiological act ivi ty of bivalves and, asconsequ ence , the e ff i ciency of accum ula t ion of bac tr ia . For four species of bivalvesM. arenaria, Pro-tothaca staminea, Crassostrea gigas,and Mytilus edu-lis), a pos i t ive cor re la t ion be tween the uptake ocol i form bac ter ia and tempera ture has been founM usse l s m ore in tens ive ly accum ula ted bac te ria l ce l ls17~ than a t 7-12~ whi le , for the o ther three spec iof mol lusks , the accum ula t ion peak was a t 12~ anthe in tens i ty of ce ll capture was mark edly redu ced 17~ Thus , the accumula t ion of bac te r ia var ies wiseason [32] , and, moreover, in the musselM. gallopro-vincialis,th is process i s favored by the decreased sa l ini ty and increase d turbidi ty o f seaw ater [31 ] .

At the sam e t ime, there is no consen sus in the l i te

a ture on the e ffec t of the concent ra t ion of bac te r ia omol lusks re tent ion e ff i c iency. Some authors be l i evthat the uptake o f bacter ial cel ls by mo ll lusks has a spc i f ic threshold , w hich i s a func t ion of the concent ra t iof b ac te r ia in water, and tha t envi ronm enta l contamint ion is posi t ively correlated w ith the bacter ial contamnat ion of mol lusks . Cabel l i and Heffeman [35] , whs tudied the accumula t ion ofE. coliby Mercenaria mer-cenaria, demons t ra ted tha t the re la t ionship be tweemol lusk contamina t ion (y) and the concent ra t ion bacter ia in seaw ater (X) is descr ibe d by the equ at ion y0 .96X + 0 .97 . A s imi la r cor re la t ion was found for tm usse l M. galloprovincialisf r om t he Med i t e r r anean

Sea [31]. H owever, a fa i r y we ak re lat ionship be twethe adsorpt ion o f co l i form bac ter ia and the i r concent rt ion in seawater was foun d for four spec ies of b iva lvM. edulis, C. gigas, M. arenaria, and P. staminea[32].

Exper imen ts on a r ti f ic ial contamina t ion o f m ol lushave demons t ra ted tha t the uptake of bac te r ia i s thhig hes t at the initial stage, w ithin the first 2--6 h o f ft rat ion. Thus, in one s tudy, the musselM. edulisremo ved 90 of H3- thym idine- labe l ledE. c oil, Staphy-lococcus au reus, Micrococcus luteus, M. cereus,andBacilus cereusce l l s wi th in 2 h [33]. According to Bernard [32], the in i t i al per iod o f the m os t in tens ive acc

RUSSIAN JOURNAL OF MA RINE BIOLOGY Vol. 26 No. 2 20 00


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ROLE OF BIVALVES IN THE DEPURATION OF SEAWA TERS 8

mula t ion of co l i form bac ter ia byM. edulisis 3 to 4 h.In addi t ion , there i s ev idence tha t the m aximum contentof enter ic bacter ia in this mollusk is al ready observedaf te r 30 min of exper imenta t ion . I t has been empha-sized that this accum ulat ion eff iciency of bacter ial cel lsis direct ly related to the concentrat ion of bacter ia inseawater, which, in the s tudy in quest ion, var ied from4 x 101-3 x 107 cells/m l (cited after [70]).

A study o f the f i lt ration of the enter ic b acter iaE. coliby V. verrucosa showed that , wi thin the f i rs t 4 h ofexper imenta t ion , the mol lusk removes 47 .3 of thecel ls , wh i le , during the sub sequent 20 h, the concen tra-t ion of bacter ia gradual ly decl ines, reach ing a plateau.For the M edi te r ranean musse lM. galloprovincialis,theremoval eff iciency ofE. coli cells in the initial 4-hperio d is stil l high er, at 96.6 [39]. InC. virginicaandMercenar ia campechiensisplaced in an experimentaluni t , the maximum amount of the bac te r iaVibriovulnificusand V. cholerae i s non-observed af te r 6 h o fexperim entat ion [72] . The oy sterC. gigasdecreases theconce ntrat ion of C~4-1abel led natural bacter ioplankton

almo st by half within the f irs t 1.5 h of experim entat ion,but the fil tration rate drops drastically later on [26]. Atthe sam e t ime, there is evidence that the ini t ial s tage ofrapid accumulat ion of bacter ia by mollusks, oysters inpart icular, i s protracted. Thus, in exp erimen ts with oys-ters ar t i ficially contam inated with p32 and Ig~cul tures of en te r ic bac i ll i, the max imum uptake of bac-ter ia by o ysters occurre d within i 8 h and de cl ined grad-ual ly over the next two d ays. The u ptake eff iciency wasdepend ent on the t empera ture and sa l in i ty of the seawa-ter [76].

After the fai r ly intensive ini t ial s tage o f adsorpt ionof bacter ial cel ls , this proc ess can b e retarded, level l ingoff to a plateau, when i t i s compensated for by thedigest ion or el iminat ion of intact bacter ia via feces orpseud ofeces [32].

Localizat ion o f Bacterial Cellsand Thei r Subsequent Fate

Bacter iological analyses indicated that the degre e ofcontamina t ion var ies among b iva lve organs , sugges t ingthe i r regular dis t r ibut ion of absorbed bacter ia withinthe bivalve body. In m ussels and oy sters , the contractormuscle, mant le , and gi l ls are, as a rule , the least con-tamina ted , whi le the h ighes t number of bac te r ia i sf ound i n t he o rgans connec t ed wi th f ood d i ges t i on - - t hegut and hepatop ancreas [38, 56, 64] . Specif ically, in themusse l M. edulis,75 to 95 of the bacter ia are local-ized in the digest ive t ract and stom ach, wh ile the m an-t le , gi l ls and other t issues, which make up 80 of thebody mass, contain a smal l number of bacter ial cei ls[70]. In the oysterC. gigas, a lmost 90 of the he t -e ro t rophic bac te r ia and up to 93 of the col i formmicroorganisms captured f rom the envi ronment a refoun d in the digest ive t ract , mainly in the s tomach a ndhindgut . Col i forms usua l ly accumula te in the s tomach(85 ) , whi le their proport ion in the digest ive diver t ic-

u lum i s much lower (3 .4 ) . Hetero trophic bacte r ia amost ly loca l ized in the s tomach and h indgut (47 an42 , r espec tive ly). W hi lePseu d o mo n assp a re foundin almost al l t issues and organs,Vibrio sp andAcineto-bacter sp are chief ly isolated fro m the digest ive t ractthese bacter ia acco unt for 44 of the bacter ial isolaof the s tomach, 68 in the crystal l ine s tyle , 72 in thdigest ive diver t iculum , and 81 in the hindgu t . Thn u m b e r o fPseu d o mo n assp decreases f rom 27 in thes tomach to 0-3 in the c rys ta ll ine s ty le and h indgut the o yster [56].

In the oys te rC. rhizophorae,wh ich is used as a bio-logical indicator of bacter ial contaminat ion of natursea waters , heterotrophic bacter ia accumulate in thdigest ive gland and the poster ior intest ine; the domnant spec ies a re representa t ives of the Pseudomondacea e- - so l i t a ry bac i l li form cel l s of 0 .5-1 x 1 .5-4 ~[38]. In M. edulis mussels ar t i f icial ly contaminatedwi th E. coli, up to 94 of th i s co l i form occurs in thedigest ive t ract . These microorganisms are found much smal le r numbers in the g i l l s , musc les , an

haem olym ph [68]. Cabel l i and Heffernan [35] point othat V. verrucosaaccumu la tes mos t of i ts captured bacterial E. coli cel ls in the s iphon t issue and digest ivgland. Studies on the condi t iona l ly pa thogenic m icrolora of the scal lopPecten pecten,which were car r i edout on oys te r fa rming grounds in four b ight s in Pe tthe Grea t Bay (Sea of Japan) , showed tha t the h ighenum ber (9 out of 12 spec ies ) of bac te r ia of the geneAeromonas, Pseudomonas, Vibrio,and some othersoccurs in the hepa topancreas , the organ tha t accumlates m icroflo ra mo st intens ively [1 ].

Thus, m ost authors con clud e that the greater par t bac te r ia remov ed by m ol lusks f rom the envi ronmentthe f i l t rat ion process are f inal ly introduced into thdigest ive system.

The subsequent fate of bacter ial cel ls captured bmol lusks i s am biguous : e i ther they a re d iges ted in tdigest ive system of mollusks, or, not being subject lysis and rem aining v iable, they are agglut inated in twaste m ater ial of the mo llusks and thus returned to tenvironment . The lat ter appl ies to bacter ia which, fone reason or other, do not enter the intest ine and ae l imina ted f rom the organism via the pseudofecwh en in con tact with the epi thel ial t i ssues in the m ancavity.

The examples of how bac ter ia offe red as food adul t and larval bivalves are digested in the bivalstomach are many and pertain to var ious species [369] . In par t icular, the s tudy of t ime-co urses in the retetion of C 14- and C51-1abeiled bacter ial fo od by the mlusks Potamocorbula am urensisand Macoma bal t icareveals that , in the course of digest ion, the feces aexpel led in two port ions. The ex pulsion o f the f irst pt ion of feces is l inked to the com plet ion of the extraclular digest ion cycle in the intest ine, whi le the secois associated with the intracel lular digest ion of bactein the hepatopan creas. I t has been noted that int racel



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lar d iges t ion of bacter ia l food i s p revalen t inP. amu ren-sis whi le ex t racel lu lar d iges t ion i s p revalen t inM. bal-tica [41 ].

The ro le o f bacter ia in the feed ing of mol lusks i sdual : bacter ia p rov ide an add i t ional source o f p ro te inand a id in the d iges t ion process [69]. Prel iminary dataon the fa te o f cer ta in h igh po lym er const i tuen ts o fbacterial cel ls suggest that extracts from the digest iveg l an d o f t h e m u sse lM. edul isdest roy lysozyme-sensi -t ive microorgan isms, and bacter ia wi th lysozyme-sen -s i t ive cel lu lar wal l s rap id ly degrade in the mol luskintest ine. On the basis of exper imen tal data, the authorscalculated the in gest ion rate of these bacteria, 2 x 108to 27 x 10s cel ls / ( ind h) . At the sam e t ime, lysozym e-sensi t ive bacteria such as Micrococcus roseusS. aureus an d B. cereuswere e l imin a t ed f ro m th e mu s-sel o rgan ism in the in tact fo rm [33] . Ment ion shoulda l so b e mad e o f t h e wo rk o f Ch ar leset al. [40] con-cerned wi th the f i lt ra tion ofE. colibacter ia by the mol-lusks V. verrucosa and M. gaUoprovincialis. Th eau thors const ructed m athemat ical m odels o f f i lt rat ion

by these mol lusks , s imulat ing the d is t r ibu t ion of arad ioactive label betw een the m ol lusk ' s body, d isso lvedand p art iculate organic matter, CO 2, feces, and pse ud-ofeces . The ass imi la t ion of bacter ia l ce l ls by the m ol-lusks was fair ly low, at 11.1-20.4% forV. verrucosaan d 7 .5 -1 4 .8 % fo rM. galloprovincialis.

Agglut inat ion o f Viable Bacter ial Cel lsin Mol lusk Feces and Pseudofeces

Con com itan t wi th the accumulat ion of microorgan-isms in the m ol lusk ' s body and thei r des truct ion in thedigest ive system , the bacterial cel ls not subject to lysis

and re ta in ing v iab i l ity are re tu rned to the env i ronmen t .This p rocess can o ccur in the mo l lusk gas tro in tes t inalt ract and terminate in the e l iminat ion of cap tured bac-ter ia wi th the feces and th rough the g i l l apparatus ,wh ere the re ta ined par t ic les are agg lu t inated by mucu sand then e l iminated v ia pseudofeces . For example , inM. m ercenar iamollusks ar t if icia lly con tam inated w i thE. coli and Salmonel la typhimur iumbacteria, the lat terare relat ively rapidly el iminated within the f irst 8 h ,af ter which p o in t the p rocess i s re tarded . Af ter 24 h , thedensi ty o fE. coli decl ines to a g reater degree than thato f S. typhimurium. Thebacter ia l ce l l s are washed ou t o fthe mol lusk organ ism, being a t tached to the rap id lydeposi ted fecal and pseudofecal par t ic les wi th whichthese bacter ia are usual ly associa ted . N o ion ic bond i sinvolve d in this ass ociat ion [78].

Data on the conc en t ra t ion of v iab le bacter ia l ce l ls inso l id waste vary among mol luskan species ; however,m ost invest igators agree that these values are insignifi-can t com pared to the degradat ion ra te o f m icroorgan-isms. Thus , d esp i te the fa i rly h igh concen t ra t ion of bac-ter ia in the feces o fM. galloprovincialisunder exper i -mental condi t ions ( the number o f hetero t rophicbacteria is as high as 10s cel l s /g and of co l i fo rms,l0 s cel l s /g w et weigh t ) , the cumulat ive conce n t ra t ion

of microorgan isms in feces and pseudofeces i s noabove 2-3 % of thei r quan t ity in the vo lum e of water ftered by a mo l lusk in 1 h . In th is even t , the con tamint ion of aggregated w aste m ater ia l was d i rect ly p ropot ional to the number o f bacter ia in the env i ronme[ 11 ]. I n the m ollu sk V.verrucosa place d in a f i l trate ofC~4-1abelled bacterial cu l tures, 8 .8% of the radioactilabel is el imina ted with the fe ces [30].

Mol lusk feces and pseudofeces p rov ide a pecu l isubstra te fo r the develop men t o f bacter ia, p ro tozoanand o ther aquatic o rgan isms. As a conseq uence, molusk b iodeposi t s can subseq uent ly affect the con ten t sed iment o f o rgan ic mat ter, includ ing an thropogenmaterial , and f inal ly the quali ty of the m arine envirom ent [19].

I t has bee n exper im ental ly shown that m ost bacterconcen t ra te on the surface o f aggregated waste m atr ia l, being adsorbed by the mu cous substances o f tenve lope. This appears to be true o nly for the ini t irevers ib le s tage of adsorp t ion of microorgan isms on tsur face o f fecal par t ic les because, dur ing ac t ivmec hanical act ion that can des t roy the envelopes , 61 77% of the bacter ia l ce l l s con tained in feces m ay reveto a suspended s ta te w i th in 24 h o f exper im ent [11This p rocess a l so largely decreases the posi t ive ro le the se d imentat ion of a l loch thonic bacteria v ia aggrgated mol lusk waste , the microf lo ra o f w hich can susequent ly be u t i l ized by det r i tus feeders dwe l l ing the bo t tom.

The Sani tary and Bacter iological Role o f Bivalvesin the Aquat ic Envi ronment

Ow ing to thei r h igh f i l tra tion capacity, com mo n spcies o f bivalves are re garded as biofi l ters act ively pat icipat ing in the transform ation of part iculate m atterthe coastal zone of the sea. Th e term biofi l ter was f ip roposed by V oskresensk i i fo rM. edul isf ro m th e Wh i t eSea [7] . I t was suggested that the fou l ing b iocenosiscoastal water areas be regarded as a bel t of f i l terio rgan isms. Later on , Bervald [3 ] work ed ou t a methfor the b io log ical pur i fication of r iver waters con tain iexcess ive quan t i ties o f o rgan ic and mineral par t ic lus ing specia l tanks in which were p laced f reshwatb ivalves o f the genusAnodonta . He poin ted ou t thattanks can successfu lly be rep laced by a natural fou l i

b iocenosis on ex t ra surfaces o f var ious hydro techniconst ructions . In th is regard , we men t ion a la ter woon the ro le o fAnodonta piscinal isin the addit ionalpur i fication of wastewater f rom a duck farm in L ietu[29]. In al l series of the ex perim ent to invest igate tf i lt rat ion capaci ty o f un ion ids , the mol lusks main ta inthei r normal physio log ical s ta te and d isp layed the abi ty to c lear the w ater o f bo th e xcess ive microf lo ra aparticulate organic matter.

In the las t decades , the concep t o f speci f ic use b ivalves fo r the add i t ional pur i f icat ion o f w astewaand the b io log ical mel io rat ion of the mar ine env i ro

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ment has ga ined much recogni t ion [21 , 25 , 42 , 46 , 57 ,74 , 79] . In a num ber of count r ies , these sc ien t i f ic deve l -opments have been appl ied in prac t ice [58 , 59] . In sodoing , there i s a t endency for the use of t rea ted andunt rea ted was tewater in agr icu l ture and aquacul ture toinc re a se i n bo th d e ve lope d a nd de ve lo p in g c ou n t r i e s[48] . A la rge body of publ ica t ions i s genera l ly con-c e r ne d w i th t he p r ob l e ms o f u t i li z a ti on o f mo l lu sks f o rt he pu r i f ic a t ion o f t he a qua t i c e n v i r onm e n t c o n t a in in gexcess ive quan t i t ies o f o rganic mater ia l , minera l par t i-cles [2, 16, 18, 19, 57, 71] , and heavy metals [23, 25] .At the same t ime , there a re s t il l fa ir ly few s tud ies of thevar ious aspec ts o f the use o f f il t e ring mo l lusks to lessenthe bac te r ia l contam ina t ion of insh ore sea a reas .

In Russ ian- language l i t e ra ture concerned wi th thep r ob l e ms o f s a n i t a r y b ioa me l io r a t i on o f t he ma r in ee nv i r onme n t , t he r o l e o f t he musse l sM. edulis a n dM. galloprovincialis has been ex tens ive ly explored ;how e ve r, t he u se o f o the r c om mo n spe c i e s o f b iva lv e sfor these purposes has been poor ly inves t iga ted . Thehigh poten t ia l o fM. galloprovincialismusse ls cu l t i -

va t e d on c o l l e c to r s f o r t he e nha n c e m e n t o f t he ma r in eenvi ronment in the coas ta l a rea near Odessa has beenrepor ted . Despi te the fac t tha t the a rea of observa t ionw a s c on t i nuous ly c on t a mina t e d by he a vy d i s c ha rg e s o fdom e s t i c s ew a ge , t he pa s sa ge o f w a t e rs t h r ou gh a n um -ber of un i t s o f the Ri f mus se l mar icu l ture ins ta l la tionreduce d the bac te r ia l con tamin a t ion (p < 0 .05) in 76%of the cases . Wi th a fa i r ly h igh leve l o f seawater con-t a mina t i on by he t e r o t r oph i c m ic r oo rga n i sms ( 10-s-1 7 cel ls / l i ter) and col iforms (102-104 cel ls / l i ter) , themax imal p os i t ive e ffec t o f b ioam el iora t ion was as grea tas 87 and 92%, respec t ive ly, wi th average va lues forma ny ye a r s o f obse r va ti ons be ing 43 - 5 2 % [ 13] . T h e

remov al e ff ic iency of bac te r ia a t the m iddle depth hor i -zon (5 m ) was cons is ten t ly h ig her than in the near-bot -tom layer (9 m) ; the num bers of bac te r ia in the waterdecreased , on the average , by 52 .3 and 33 .7% for he t -e r o t roph i c m ic r oo rga n i sm s a nd by 65 .1 a nd 4 4 . 0% f o rco l i form bac te r ia , respec t ive ly. These d i sc repanc ieswere pr imar i ly due to depth- re la ted d i ffe rences in thenumbe r a nd b ioma ss o f musse l s on c o l l e c to r s ; up t o47% of the overa l l b iomass occur red in the upper por-t ion of the m ar icu l ture un i t and on ly 18 .5% in the near-bo t t om pa rt . T he c l e ar a nc e c a pa c i ty o f R i f ' w a sinverse ly re la ted to the contamina t ion of the envi ron-ment and bac te r ia l p ressure on the mol lusks . Usua l ly,

hard ly any e ffec t is found (10 .3% of cases) wi th lowf low ve loc i ty and s low water m ot ion , which a re charac-ter is t ic of 9- to 10-m depths. I t is not possible to s tatewi th fu l l assurance tha t the b ioam el iora t ion e ffec t isequa l to 0 , bec ause m ol lusk s can repea ted ly f i l t er asma l l vo lum e o f w a t e r imme d ia t e ly a d j a ce n t t o t he m.The c learance e ff ic iency may even increase , bu t thevo lume o f w a t e r i n t he de pu r a t i on l a y e r w i l l r e ma inl imi ted .

The ab i l ity of b iva lves to accum ula te var ious micro-f lora in their organs can be a real hazard to potent ialcon sum ers s ince mol lusks , ac t ive ly par t ic ipa t ing in the

pur i f ica t ion of the mar ine envi ronment , a re f requent lc a r r i e r s o f pa tho ge n i c m ic r oo rga n i sms a n d v i r u se sE a t i n g r a w mo l lu sk s i s o f t e n th e c a use o f f ood p o i soings , a l le rg ies , and infec t ious d i seases [75]. Thereformo l lusk mar icu l ture for the san i ta ry b ioam el iora t ion coas ta l a reas i s l imi ted becau se of the problem s of subse qu e n t u t i l iz a t io n o f he a v i l y c o n t a min a t e d mo l lu skT he e x i s t i ng r o u t i ne t e c h n iqu e s w e r e d e v i s e d f o r t hd e pu r a t i on o f mo de s t l y c o n t a mina t e d mo l lu sk s a ninvolve the i r main ten ance in spec ia l t anks or pools wic i rcu la t ing seawater p rev iou s ly d i s infec ted by u l t rav ile t rad ia t ion or ozon e over a br ie f depura t ion cyc le [472 , 78] . As a ru le , it i s hard ly poss ib le to p ur i fyM. gal-loprovincialis tha t conta insE. coli concent ra t ions inexce ss of 102 cel ls /g in the tissue ov er 1 8-2 4 h [9] . e nv i r o nme n ta l l y c o n t a min a t e dC. virginica a ndM. mercenar iamol lu sks , t he nu m b e r s o f f e c a lE. colia n d Salmonella sp c o l i f o r ms de c l i ne d t o a n un d e t e c tab le leve l wi th in 14 days [54]. Clear ly, th i s depura t iot ime i s inapprop r ia te for l a rge-sca le pur i f ica tion .

The resu l t s o f observa t ions on la rge-sca le depura

t io n o f t h e mo l lu sksM. mercenariaind ica te tha t depu -ra t ion e ff iciency i s en t ire ly dep end ent on the leve l c on t a min a t i o n o f m o l lu sk s , a n d t ha t t he i r fu l l de p u rt ion over 24 h can occu r on ly a t an in i t ia l concent ra t io f E. coli not above 102-103 ce l l s /100 g sof t t i s suh om o ge n a t e . I n c a se t he i n it ia l c on t a mina t i on o f m olusks i s g rea te r than 105 ce l l s /100 g , on ly 40% of tmo l lu sk s a r e de c o n t a m ina t e d w i th in a 48 - h d e p u r a t iper iod [49] . More e ff ic ien t methods , such as oxygehy d r o ly s i s o r h igh t e mp e r a tu r e d r y ing , sh o u ld p r o b a bb e u se d w i th h e a v i ly c o n t a m in a t e d mo l lu sk s f o r thsa fe e l im in a t io n o f p a tho ge n i c m ic r o f lo r a . T h e hy d rlyza tes can be u t i l i zed in the pharmaceut ica l indus ta nd f o r t he p r od uc t i on o f v a r iou s m e d i c in e s , w h i l e tf lour provides a va luable food su pple me nt for l ives toc

T he u se o f c o m mo n sp e c i e s o f b iva lv e s f o r impr oing the san i ta ry and bac te r io log ica l charac te r i s t ics the sea requi res en t i re ly nove l type s of mar icu l ture colec tors to be devised . Th ese sy s tems m ust d i ffe r accoring to the func t ion to be fu l f i l l ed : the e l imina t ion a l l oc h tho n i c b a c te r ia i n z on e s o f c o n t i n uous d i s c h a rof domes t ic and indus t r ia l sewage or the addi t iondepu ra t ion of recrea t ion zones of the sea [6]. To reso lt h e p r o b l e m o f e f f ic i e n t u se o f mo l lu sk s f o r t h e b io a ml iora tion of insho re a reas of the sea and for increas i

the pur i f ica t ion po ten t ia l o f the mar ine envi ronmenextens ive s tud ies in sea a reas wi th d i ffe ren t bac te r ipressure a re needed .

.

R E F E R E N C E S

Avdeev a, N.V. and Filipchuk, E.S., Cond itionally P athgenic Microflora of Scallops on Scallop FarminGround s in Peter the Great Bay,Vsesoyuznayakonferen-tsiva po morsko i biologii, Sevastopol , O kt. 1988: Tedokladov (Abstracts of Papers, All-Union Conf. oMarine Biology, Sevastopol, Oct. 198 8), Kiev , 198part 2, p. 47.

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6/8


7/8

ROLE OF BIVALVES IN THE DEPURATION OF SEAWATERS 87

the U SSR, 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 ofWastewater from Duck Farms, Biologicheskie resursyvodoemov basse ina Ba l t i i skogo morya , Mate r i a ly XXInauchnoi konferentsi i po izucheniyu vodoemov Pr ibal -t iki (Biological Resources of Water Bodies of the BalticSea 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 contaminationbact6rienne des moules: essai de mise au point d'un testrepr6sentatif 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 o f 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. Ep idemio l .,1977, vol. 105, no. 4, pp. 337-343.

35. Cabelli, V.J. and Heffernan, W.P., Accumulation ofEscher ichia col iby 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 Myti lus edul is , Invest . Pesq. ,1966, no. 30,pp. 639-65 i.

37. Castro, A., Gonzalez, J., Espeleta, C., and Carrera, J.,Presencia de Salmone l l aen 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 (Crassost rea rhizophorae) eaguasda 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 Escher i ch iacoli by Two Filter-Feeding Bivalves, Venus ver rucosaand Myti lus gal loprovhtcial i s .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 Escher ichia col ibyTwo Filter-Feeding Bivalves, Venus ver rucosaand Myt i -

lus gal loprovincial is .II. Modelling, Ma r. Bio l . ,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-bu la amurens i sand Macoma bal t ica:Significance to theAdsorption of Carbon and Chromium, Mar. Ecol. Prog.Ser., 1991, vol. 78, no. 3, pp. 303-314.

42. Devik, E.O., Hatvest ing Pol luted Waters . Waste Heata l ~ Nut r i en t - loaded E ff luen t s in the Aquacu l tu r e ,NewYork: 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 virginicaGmelin), J. Gen. Physiol. ,1928, no. I l, pp. 415-431.

45. Gauthier, M.J. and Brittymayer, V.A. , La pollutionbact6rienne de lamer, Recherche ,1990, vol. 21, no. 223,pp. 910-912.

46. Gomoiu, M.-T., Potential Role and Ecological Effects ofArtificial Reefs Constructed on the Coastal Sandy Bot-tom of the Black Sea (Romania), Trav. Mus. H ist. N atur.

"Gr. Ant ipa , " 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 . Repor t Ser. WHO,1989,no. 778.

49. Heffernan, W.E and Cabelli, V.J., The Elimination of Bac-teria by the Northern Quahaug: Variability n the Responseof 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 Myti lus edul isin Different Kinds of Suspension, J. Mar. Biol. Ass. U .K.,1949, no. 28, pp. 333-344.

51. J6rgensen, C.B., Efficiency of Particle Retention andRate of Water Transport in Undisturbed Lamellibranchs,J. Cons. hzt. Explor. M er. ,1960, no. 26, pp. 94--116.

52. J~rgensen, C.B., Famme, P., Kristensen, H.S., et a l . , Th eBivalve 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 Evaluationof Relaying for Purification of Contaminated Shellfish,87th Annu al Me et ing o f the Am . Soc. Microbiol ., At l1-6 March, 1987,Washington, D.C., 1987, p. 301.

55. Kemp, P.F., Neweil, S.Y., and Krambeck, C., Effect ofFilter-Feeding by the Ribbed Mussel Geukens ia demissaon the Water- Column Microbiota of a Spar t ina al terni -f lo r a Saltmarsh, M ar. Ecol . Prog. S er. ,1990, vol. 59,nos. 1-2, pp. 119-131.

56. Kueh, C.S.W. and Chan, K.-Y., Bacteria in BivalveShellfish with Special Reference to the Oyster, J. Appl.Bacter iol . ,1985, no. 59, pp. 41--47.

57. Larsson, A.-M., Blue Mussel Sea Farming--Effect s onWater Quality, Vatten, 1985, voi. 41, no. 4, pp. 218-224.

58. Mann, R. and Taylor, R.E., Jr., Public Health Aspects ofthe Culture of the Japanese Oyster Crassos t rea g igasina Waste Recycling Aquaculture System, Aquacul ture ,1983, vol. 30, nos. 1--4, pp. 311-327.

59. Martin, Y., Bonnefont, J.L., and Guinnet, B., Risquessanitaires li6s a I'utilisation des effluents urbains enaquaculture marine, Techn., Sci. , Meth.,1990, no. 9,pp. 413--420.

60. Mason, J.O. and MacLean, W.R., Infectious HepatitisTraced to the Consumption o f 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


8/8

8 8 G O V O R I N

62. Metcaif, T. and Stiles, W., The Accumulation of theEnteric Viruses by the OysterCrassostrea virginica,J. Infect. Dis.,1965, no. 115, pp. 68-7 6.

63. Me yer-Ro chow , V.B., Observation s on an AccidentalCase of Ra w S ewag e Pollution in Antarctica,Zbl. Hyg.Umwel tmed . ,1992, vol. 192, no. 6, pp. 55 4-55 8.

64. M inet, J., Barbo sa, T., Prieur, D., and Cormier, M ., M iseen 6viden ce du proc essus de concentration des bact6riespar la mouleMytilus edulis, C. R. Acad. Sci. (Paris),

Ser. III, 1987, vol. 305, pp. 351-354.65. MO hlenberg, E and Riisgard, H .U., Efficien cy of Particle

Retention in 13 Species of Suspension Feedin g Bivalves,Ophelia , 1978, no. 17, pp. 239-246.

66. Olacz yk-N eym an, K., Mik robiolog iczne aspekty zaniec-zyszczenia w6d morskich c iekami,lnz. Mor., 1980,vol. 1 , no . 11 , pp . 390 -391 ,393 -39 5.

67. Owen, G., Feeding and Digestion in the Bivalvia,Adv.Comp. Physiol . Biochem. ,1974, vol. 5, pp. 1 -35.

68. Pow er, U .E an d Collins, J.K., Tissue Distribution of aColiphage andEscherichia coliin Mussels a f ter Con-tamination and Depuration,Appl. Environ. Microbiol. ,1990, vol. 56, no. 3, pp. 803-8 07.

69. Prieur, D., Nou velles donn6s sur relations entre bact6deset b ivalves m arins,Haliotis, 1981, no. 11, pp. 251 -260 .70. Prieur, D., Mevel, G., Nicolas, J.-L.,et al. , Interactions

between Bivalve Mollusks and Bacter ia in the MarineEnvironment, Oceanogr. M ar. Biol. Ann u. Rev. ,1990,no. 28, pp. 277-352.

71. Rod house , P.G. and Rode n, C.M., Carbon B udget for aCoa stal Inlet in Relatio n to Intensive Cultivation of Sus-pension-feeding Bivalve Mollusks ,M ar . 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., U ptake , Fate and Elimination by Shellfish in aLabora tory Depura t ion System,Oc eans 87 Proceed-

ings, Ocean-Int. Workplace, 1987,Ne w York, 1987 ,vol. 5, pp. 1752-1756.

73. Spittler, P., de la Alfred o, C.S., Rodriq uez, J., La selecion del tam a6 de las particulas alimenticias po r el ostiCra ssostrea rhizophorae, R ev . Invest. M ar. ,1989,vol. 10, no. 1, pp. 63 -70 .

74. Stirn, J., Pokleka, D., and Vukovic, A., Ciscenje komnalnih v oda z reciklazo v marikulturah,Hem. Ind. ,1977,vol. 31, no. 7, pp. 357-360.

75. St6ven, K ., Krank durch M uschelgenu ,Lebensmit-teltechnik, 1980, vol. 12, no. 1 I, pp. 26 -29 .

76. Takase, A. and Bito, T., The Utilisation of Radio isotoLab elled Bacte ria in the Fo od Sanitation Studies. III. Othe Bacterial Contamination of Living Oysters,Preprintof the 4th Japan Conf. Radioisotopes (JRIA),1961.

77. Tammes, P.M.L. and Dral, A.D.G., Observa tions on tStraiting of Suspensions by Mussels,Arch. Ned. Zool. ,1955, vol. 11, pp. 87-111.

78. Timoney, J.E and Abston, A., Accu mu lation and Elimnation ofEscherichia coliand Salmonella typhimuriumby Hard Clam s in an In Vitro System ,Appl. Environ.Microbiol. ,1984, vol. 47, no. 5, pp. 986 -988 .

79. Utilisation of Sew age Effluent for Shellfish Culture,FAOAquacult. Bull. ,1972 , vol. 5, no. 1, p. 4.80. deVilliers, C.J. and Allanso n, B.R ., Efficiency o f Partic

Retention in Solen cylindraceus(Hanley) (Mollusca:Bivalvia), Estuar. Coast. ShelfSci. ,1988, vol. 28, no. 4,pp . 421-42 8.

81. Wright, R.T., Coffin, R.B ., Ersing, C.P., and Pearson, DField and La boratory M easurem ent o f Bivalve Filtratiof Natural M arine Bacterioplankton,Limnol. Oceanogr. ,1982, vol. 27, no. 1, pp. 91-98.

82. ZoBell, C.E. and Feltham, C.B., Bacteria as Food fCertain Marine Invertebrates, J.M ar. Res. ,1937, no. 1,pp . 312-327.


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