1 a 1 I = I - Integrative and Comparative Biology

AMER. ZOOL., 36:364-372 (1996)

Osmotic and Ionic Regulation of North American Zebra Mussels{Dreissena polymorpha)1

THOMAS H. DIETZ, SHAWN J. WILCOX, ROGER A. BYRNE*,

JOHN W. LYNN, AND HAROLD SILVERMAN

Department of Zoology and Physiology, Louisiana State University,Baton Rouge, Louisiana 70803 and

*Department of Biology, SUNY, Fredonia, New York 14063

SYNOPSIS. Unlike other freshwater bivalves that survive for months indeionized water, Dreissena polymorpha requires minimal concentrations ofNa, K, Mg, and Cl in the bathing medium for long-term survival. Althoughion transport rates are higher in D. polymorpha compared to other fresh-water bivalves, they tend to have lower blood solute concentrations. D.polymorpha has an unusually "leaky" epithelium with a high paracellularpermeability to solutes. Thus, even with high transport rates, it may not bepossible for zebra mussels to retain higher blood solutes because of theextensive passive loss of ions. Under a hyperosmotic stress, D. polymorphawill rapidly osmoconform (about 12 hr) due primarily to the diffusion ofsolutes and partially to the osmotic loss of water. D. polymorpha is notcapable of surviving an imbalance of Na/K in the external medium. In theabsence of K the cells will tend to lose volume to achieve isosmotic balancewith the blood, but the animals usually die within a few days. If D. poly-morpha is exposed to excess K in the environment (1 mM), they willaccumulate K in the blood. If the K enters the cells, cellular volume wouldexpand due to increase in osmolyte concentration, yet, if K remains in theblood, there will be an electrochemical imbalance. In either case, the animalcannot survive much longer than a day. When Na and K are present in themedium in a balanced combination approximated by artificial seawater(ASW), D. polymorpha will survive an acute transfer to 100 mosm ASWindefinitely (months). Our preliminary studies have shown that D. poly-morpha will tolerate step-wise acclimation to solutions >250 mosm pro-vided the changes in salinity do not exceed 50-100 mosm. Freshwaterbivalves, unlike the marine bivalves, have limited free amino acids in theirbody fluids and must rely on inorganic ions for osmotic regulation. Thefree amino acids serve as an important osmolyte buffer for volume regu-lation when an animal experiences an environment of changing salinity.The inability of Dreissena, and perhaps other freshwater bivalves, to tol-erate hyperosmotically induced dehydration may be due, in part, to theinability to accumulate or retain sufficient intracellular K to facilitate reg-ulatory volume adjustments.

INTRODUCTION in the fresh waters of North America. D.Dreissena polymorpha (zebra mussel) is polymorpha also represents a bivalve group

the most recently (1986) introduced bivalve that has invaded freshwater in recent geo-logic history (McMahon, 1991; Nuttall,

1 From the Symposium Biology, Ecology and Phys- 1990). This review will provide some COm-iology of Zebra Mussels presented at the Annual Meet- parative data On OSmoregulation by dreis-ing of the American Society of Zoologists, 4-8 Janu- s e n i d s and o t h e r freshwater bivalves, andary 1995, at St. Louis, Missouri. ... . ,. , ,. . . , .

' Address Correspondence to: T. H. Dietz, Depart- Wl11 C O n t a i n S O m e r e C e l U unpublished datament of Zoology and Physiology, Louisiana State Uni- from Our laboratory. We have attempted toversity. Baton Rouge, LA 70803. be complete, but have limited a review of

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IONIC REQUIREMENTS AND SALT TOLERANCE 365

literature because of the constraints of thisforum. A significant number of studies arecited in the recent bibliographic data basepublished by Schloesser et al. (1994).

Zebra mussels are similar to other fresh-water (FW) bivalves in that they are hyper-osmotic regulators, yet all FW bivalve spe-cies maintain a very low concentration ofblood solutes (38-65 mosm) (Table 1).Some of our recent studies have providedsurprising results suggesting that dreissenidepithelia are unusually "leaky" allowingmolecules as large as 5,000 Da to passthrough paracellular pathways. The leaki-ness of the epithelia may be one of the fac-tors that contributes to the exceptionallylow blood solute concentrations, at least inthe dreissenids. Although similar osmoti-cally, the ionic composition of the blood offreshwater bivalves differs between species.The dreissenids and Corbicula fluminea(Corbiculidae) have blood that is primarilya NaCl fluid with rather small amounts ofHCO3 (Table 1). The blood of other bi-valves (margaritiferids, unionids, andsphaeriids) contains higher concentrationsof HCO3. The values listed in Table 1 forblood ion concentrations are representative.We have observed that blood total solute inCarunculina texasensis ranges from 35 to50 mosm, and specimens of D. polymorphafreshly collected from the Mississippi Riverin the summer is about 30 mosm to over 50mosm in winter.

Although bivalves have low ion concen-trations in the blood, they have ion trans-port characteristics similar to other FW an-imals (Dietz, 1979). Freshwater bivalvesare able to transport Na from Cl-freeNa2SO4 solutions (Table 2). The dreissenidsexhibit higher transport rates than many ofthe other FW bivalves. Similar studies alsohave shown that Cl transport is independentof Na in FW bivalves (Dietz, 1979; H.Zheng, LSU, unpublished observation).Some of the apparently high transport ratesobserved in Dreissena may be due to dif-fusive uptake, as discussed in more detailbelow (Wilcox and Dietz, 1995).

SPECIFIC ION REQUIREMENTS

Several investigators have noted thatdreissenids are sensitive to the chemical

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366 T. H. DlETZ ET AL.

TABLE 2. Unidirectional Na fluxes in pondwater acclimated bivalves in 0.5 mM Na2SOj.

Species

Margaritifera hembeli'Carunculina texasensis*Corbicula fluminea*Musculium transversum"Dreissena polymorpha*'D. bugensisb

aDietz, 1979; b T. H. Dietz,

mass, g

1.43 J0.10 i0.07 i0.02 i0.04 i0.04 j

t 0.09t 0.00t 0.01t 0.00t 0.00t 0.01

unpublished observation; *

jimol (g dry

Influx

4.9 ± 0.91.4 ± 0.4

10.0 ± 2.420.7 ± 3.014.0 ± 2.7

*20.5 ± 2.4

in pondwater.

tissue-hr)"1

Efflux

1.4 ±1.5 ±8.0 ±

29.9 ±19.5 ±21.3 ±

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composition of the environment and thatthis affects their distribution and populationdensity (Ramcharan et al., 1992), embryo-logical development (Sprung, 1987), andability to survive in the laboratory (Nichols,1993; Ram and Walker, 1993; Dietz et al.,1994). It is remarkable that, for a freshwateranimal, Dreissena polymorpha cannot tol-

lon Combination

NaCI.NaHCO3.MgSO4

NaCI.CaCl2,MgSO4

NaCI,KCI.MgS04

Naa.MgS04

NaHCO3.KCI.MgSO4

KCI,NaHCO3.CaCl2.MgS04

NaCI.NaHCO3.CaCl2.MgS04

NaCl,KCI.NaHCO3,CaCl2,MgSO4

NaCI.KCI.CaCl2,MgSO4NaCI,KCI.NaHCO3,MgS04

NaHC03.MgS04

NaHCO3,CaCl2.MgSO4

NaCI,KCI.NaHC03

NaHC03,NaCI

NaHCOs.KCI

NaCI.KCI

NaCI,KCI.CaCl2

NaCI,KCI.NaHCO3.CaCl2

NaCI

NaCI,NaHCO3,CaCl2

NaHCO3

KCI.NaHCO3.Caa2NaCI.CaCI2

NaHCO3,CaCl2

KCI.MgSO4

DeknizedWaterKCI,CaCl2

CaCl2

CaCl2,MgSO4

KCI

MgSO4

KCI,CaCl2.MgSO4

0 10 20 30 40 50Lethal Time (days)

FIG. 1. Lethal time for 50% (LT ,) or 100% samplemortality (SM100) for D. polymorpha in deionized wa-ter or solutions of the salts at the concentration presentin artificial pondwater. PW salt concentrations, in mM:XaCl, 0.5; KCI, 0.05; NaHCO,, 0.2; CaCl2, 0.4;MgSO4, 0.2 (Adapted from Dietz et al., 1994).

3j DSMIOO

erate deionized water for any appreciablelength of time (Fig. 1). The lethal time for50% mortality (LT50) was <4 d and all an-imals in the deionized water died in 5 d(time for 100% sample mortality, SMJOQ).Other FW bivalves will tolerate deionizedwater for months with no mortality (seeDietz et al., 1994; Krogh, 1939; McCorkleand Dietz, 1980; Murphy and Dietz, 1976;Scheide and Dietz, 1982).

D. polymorpha has a requirement forminimal or threshold amounts of Na, K, Mgand Cl for survival in the laboratory, butthis intolerance of ion-deficient media is notobserved in other freshwater bivalves(McCorkle and Dietz, 1980; Murphy andDietz, 1976; Scheide and Dietz, 1982). Ze-bra mussels exposed to a medium deficientin Mg have an LT50 <3 weeks. The musselsexperience an exponential loss of Mg fromthe blood with a half time of about 24 hr(Dietz et al., 1994). The Mg-deficient mus-sels will re-accumulate Mg when the ion isreturned to the bathing medium. If D. poly-morpha are held in a minimal salt solutiondeficient in K, they will survive over 50days, but they lose the ability to maintainnormal ion balance (Dietz et al., 1994). The50 d K-deficient mussels, in addition to be-ing depleted of K, also lose other ions andthe total solute of the blood is less than 30mosm. The impaired ionic balance is re-versible as the mussels restored their nor-mal blood composition within 45 hr whenreturned to pondwater (PW) (Dietz et al.,1994).

SALINITY TOLERANCE

There are numerous reports of dreissen-ids being present in salinities ranging to 4—5%c in the oligohaline waters of Europe and

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125-

100-

•a

1 7 5 H

50H

2 5 -

B SM100LT50

r 100

- 75

- 50

cEo

IOC (0" 0)

[K], mM 0.50.8 1[Na], mM 45

1.5 2 3 0.5 1 1.5 260

0.5 1 1.5 275

FIG. 2. Lethal time for 50% (LT50) or 100% sample mortality (SM.o,,) for D. polymorpha acclimated to variousNaCl and KC1 concentrations in 0.7 mM MgSO4. All animals were step-wise acclimated to 30 and 45 mM NaClwith 0.5 mM KC1 for 3 d before being transferred to the solutions listed. The maximum number of animalsforming byssal attachments during the experiment was noted and converted to a percentage (n = 20 in eachtreatment) (T. H. Dietz, unpublished observation).

Russia (Klimowicz, 1958; Jarvekiilg, 1984;Lamanova, 1970; Schloesser et al, 1994).The animals tend to be smaller in highersalinities suggesting either they do not sur-vive for much longer than a year or thatthey grow slower. Oligohaline water wouldcontinually be resupplied with D. polymor-pha larvae from riverine populations. Re-cently, zebra mussels have been identifiedin tidal reaches of the St. Lawrence riverand some predict establishment of popula-tions in estuarine areas of North America(Mellina and Rasmussen, 1994; Strayer andSmith, 1993). Recent studies have shownthat D. polymorpha will tolerate dilute ar-tificial seawater (ASW) of 2-4%o (Kilgouret al., 1994). Initially, we predicted Dreis-sena polymorpha would not be very suc-cessful in saline water because of their in-ability to tolerate 45 mM NaCl, since all ofthe animals we tested died in less than aweek of exposure (Horohov et al, 1992).In contrast, other FW bivalves will toleratean acute transfer to even higher concentra-tions of NaCl for weeks with limited mor-tality.

When D. polymorpha are exposed to 45

mM NaCl, the Na and Cl ions are rapidlyaccumulated in the blood (Horohov et al.,1992). However, without an adequatesource of K, the cellular response tends tobe a volume reduction and subsequent con-centration of existing cellular K to achieveisosmotic conditions, a condition that isusually lethal within a few days (see Dis-cussion). In preliminary studies, we haveestimated intracellular space using inulinand dextran and have noted a decrease incalculated cell volume when D. polymor-pha is exposed to 45 mM NaCl. In addition,using the methods of Silva and Wright(1994) we have observed cell volume re-duction when gill tissue was exposed to hy-perosmotic conditions (unpublished obser-vation). To promote longer-term survival,Dreissena require the presence of Na andK in the medium (Fig. 2). When these mus-sels are exposed to various concentrationsof the salts that are minimally required forion regulation (Na, Cl, and K in a 0.7 mMMgSO4 solution) their survival is extended,compared to single ion challenges (Fig. 2).D. polymorpha tolerate elevated ion con-centrations when the Na:K ratio approxi-

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mates or is slightly greater than that of sea-water (45:1) (i.e., less K). The prolongedsurvival of Dreissena in these solutionswith minimal ionic components is consis-tent with the hypothesis that elevated Nacan be tolerated when there is sufficient ex-ogenous K available for cellular volumeregulation (see Discussion). Furthermore,we have observed that D. polymorpha willsurvive for months following an acutetransfer from PW to 100 mosm ASW (ap-proximately 3.5%o). Moreover, zebra mus-sels can be step-wise acclimated to >250mosm (8-8.5%©) and survive for months, ifthe increment in salinity change does notexceed 50-100 mosm (unpubl. obs.). Thevariability of response in a population ofzebra mussels exposed to hyperosmoticASW is noteworthy. We frequently observethat a substantial minority (20-30%) froma group of 20-30 mussels acutely exposedto >150 mosm will tolerate the transfer forweeks, but the majority die within days (un-published observation).

MECHANISMS OF ADJUSTMENT TOHYPEROSMOTIC ENVIRONMENTS

Recent studies indicate dreissenids areable to transport K from their environmentand the transport system displays saturationkinetics (Fig. 3; Wilcox and Dietz, 1995).The affinity coefficient for K (Km = 0.16mM) in D. bugensis is not significantly dif-ferent than that observed in D. polymorpha(Wilcox and Dietz, 1995; unpublished ob-servation). However, we observed that theestimated maximal influx (Jmax) is ratherhigh and that there is a substantial diffusiveuptake of Rb, and presumably K, in D.polymorpha. Indeed, at a [Rb] of >0.3 mM,the diffusive component exceeds the activetransport of Rb (Wilcox and Dietz, 1995).The high rate of diffusive ion uptake pro-vides some insight into how D. polymorpharapidly osmoconform to elevated ion con-centrations within 8-24 hr.

When we challenged D. polymorpha to alow ionic strength but hyperosmotic chal-lenge by adding 100 mM glucose or man-nitol to the PW, we observed that the mus-sels became isosmotic within 12 hr (Fig. 4;Dietz et al., 1995). However, contrary to anexpected increase in blood solutes due to

I/Ji

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1.

1.

0.16

1

1

5-

0 -

5-

/

//

r" — Jmax=2.23

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FIG. 3. Lineweaver-Burke kinetic analysis of K trans-port in D. polymorpha (open diamonds; adapted fromWilcox and Dietz, 1995) and D. bugensis (open cir-cles; unpubl. obs.) acclimated to pondwater and trans-ferred to pondwater with various concentrations of K.The kinetic coefficients areh~' and K^ in mM.

in u,eq g~" dry tissue

dehydration induced water loss, we discov-ered that the isosmotic condition wasachieved by the rapid uptake of mannitol orglucose through paracellular pathways.Equally surprising was the rapid loss ofions from the blood (Table 3). Under a lowionic strength hyperosmotic challenge (100mM mannitol or glucose), the paracellularroute has minimal selectivity and allowssalts to exit the animal and the non-electro-lytes to enter. From the penetration of non-electrolytes (glucose, mannitol, traceramounts of 3H-inulin), we calculated a pre-dicted blood solute composition assumingthe non-electrolytes reflect an equilibrationbetween blood and bath water. The predict-ed blood composition is the sum of 50-70% PW and 30-50% blood, and the cal-culated values for all ions are in excellentagreement with the measured blood concen-trations (Fig. 4). Under these conditions, D.polymorpha epithelia display essentially noselectivity to solutes up to 5,000 Da (3H-inulin), but penetration of I4C- or 3H-dex-tran (70 KDa) was restricted (Dietz et al.,

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Other K.Ca

Predictedvalues

100 mMglucose ~

Predictedvalues

100 mMmannitol"

Pondwatercontrol

. MgTABLE 3. Net ion fluxes over 4 h in Dreissena poly-morpha in pondwater (control) or exposed to pond-water containing 100 mM mannitol.

glucose

mannitol

25 50 75

Blood solute, mM100

FIG. 4. Effects of hyperosmotic solutions of 100 mMmannitol or glucose in pondwater on the measuredblood solute concentrations in D. polymorpha. "Oth-er" represents the difference between the total soluteand the measured solute concentrations and is primar-ily HCO3. From the specific activity of 3H inulin(cpm/u.1 bath) in the bath and the radioactivity mea-sured in the blood after 12 h treatment, an equivalentvolume of pondwater was estimated in the blood sam-ple (V). The predicted blood solute concentrationswere calculated based on a mixture of control bloodion concentrations (C,) and pondwater solute concen-trations (Co), and the solute concentrations estimatedfrom the equation: Predicted solute concentration =VCO + (1 - V)C,. Note the excellent agreement be-tween measured and predicted solute concentrations(adapted from Dietz et al., 1995).

1995). Other molluscs have been shown tohave a high paracellular permeability. Ter-restrial gastropods display high paracellularpermeability in their foot epithelium, butthere is more selectivity, or molecular siev-ing, since higher molecular weight mole-cules enter more slowly (Uglem et al.,1985).

When D. polymorpha are exposed to a100 mosm hyperosmotic and hyperionic en-vironment composed of dilute ASW, the ep-ithelial permeability is more selective (un-publ. obs.). Using 10 mM glucose, sucroseor tracer amounts of 3H-inulin as non-elec-trolyte markers of passive permeability, wefound that these markers are taken up moreslowly than that observed in the low ionicstrength experiments. Exposure to ASW re-sults in a rapid increase in the total soluteconcentration in the blood due, in part, to

Ion

NaClK

lime

Control

-0.9 ± 2.9-3.3 ± 2.8-0.2 ± 0.1

>1 (g dry tissue h)"1

Treated

-48.2 ± 10.5*-54.0 ± 13.4*-0.4 ± 0.2

Mean ± 1 SEM (n = 5). * Significantly differentfrom corresponding control ion flux using Student's t-test, P < 0.05 (adapted from Dietz et al, 1995).

the osmotic loss of water, but primarily dueto an increase in uptake of ions from thebath, probably through paracellular or otherdiffusive routes (Wilcox and Dietz, 1995;unpublished observation). In the hyperionicmedium, water apparently diffuses out andions rapidly diffuse into the mussel. Thesedata indicate that in a more physiologicallyrelevant ionic environment, zebra musselepithelia display more selective permeabil-ity characteristics and molecular sievingthan observed in mussels challenged by themore artificial hyperosmotic but low ionicstrength medium.

When D. polymorpha are exposed to 100mosm ASW they survive for months (Kil-gour et al., 1994; unpublished observation).In contrast, when mussels are exposed to100 mM glucose or mannitol in PW sur-vival is limited, with some animals dyingbetween 8-16 h and half of the animals notsurviving beyond 1.2—1.9 d (Dietz et al.,1995). The loss of ions appears to be morecritical to survival than any detrimental ef-fect due to a gain in non-electrolytes, sincesurvival is more than doubled (LT50 = 4.2d) when mussels are placed in 70 mM man-nitol with 50% clam Ringer's (70 mM man-nitol, 10 mM Na and Cl, 2.5 mM Ca, 0.25mM K, and the balance HCO3, SO4, Mg).Finally, when 1 mM KC1 is added to the 70mM mannitol and 50% clam Ringer's, sur-vival is extended to over 5 days for half ofthe animals, and 20% of the mussels sur-vived almost 3 weeks (Dietz et al., 1995).During the course of acclimation to this so-lution the animals maintain their salt bal-ance, but progressively gain additional Cain the blood suggesting they are becomingacidotic (Fig. 5; R. Byrne, unpublished ob-servations).

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mannitol + other

100n

E 75^

50HOO

CO

25H ISeea

KCl

Na

0 12 23 49 120Time, h

FIG. 5. Time course of changes in blood ion concen-trations when D. polymorpha were transferred to 50%clam Ringer's containing 70 mM mannitol and 1 mMKC1 (total solute 106 mosm). The animals becameisosmotic within 12 hr primarily due to the uptake ofmannitol. Mannitol was not assayed, but previous stud-ies have shown that most of the solute is mannitol withonly a small change in the HCO3 component of "oth-er" (see Fig. 4) (adapted from Dietz et al., 1995).

DISCUSSION

Dreissena polymorpha is the first fresh-water bivalve identified as having signifi-cant paracellular routes for solute move-ment across the epithelia. In preliminarystudies, the unionid Carunculina texasensisalso showed evidence of elevated paracel-lular permeability, but Corbicula flumineadoes not (H. Zheng, LSU, unpublished ob-servations). Perhaps the basis for maintain-ing low blood solute in some bivalves isdue to the leakiness of the epithelia. Thus,even though D. polymorpha has higherrates of ion transport than many other FWbivalves, it may not be possible to maintainblood ion concentrations at more elevatedlevels due to the persistently leaky paracel-lular pathways.

The dependence of D. polymorpha on asuitable Na:K ratio for survival in oligo-haline water is not unusual for freshwaterbivalves (see Gainey and Greenberg, 1977).However, the inability to tolerate a hype-rosmotic 45 mM NaCl challenge, when Kis less than 0.05 mM in the bathing medi-

um, is unique among the FW bivalves.NaCl is rapidly accumulated in the blood,but without sufficient K, the cells are ap-parently unable to volume regulate and themussels die. Similarly if the mussels aresubjected to additional K in the environ-ment, K will accumulate in the blood andthe mussels may not survive (Wilcox andDietz, 1995; Fisher et al., 1991). When ex-posed to elevated [K] of 1 mM, the K entersthe animal and some of the excess K maybe transferred to the cytoplasm by the Na/KATPase. This would result in excess K be-ing present in the blood, an inappropriatecell volume expansion, and disruption ofthe electrochemical balance. These condi-tions would be detrimental to an animal.

Although dreissenids have been identi-fied in many brackish water habitats in Eu-rope and Russia, they are usually confinedto lower salinity (4-5%o). The notable ex-ception was the Aral Sea that supportedpopulations of 3 dreissenid spieces, that ac-counted for 63% of the benthic biomass,until the early 1970's (Aladin et al., 1993;Williams and Aladin, 1991). Before 1970,the Aral Sea had a relatively stable salinityof about 11-12%o, but the Ca and SO4 con-centration was higher than that of seawaterand the Mg concentration was about 50%of seawater (Aladin and Potts, 1992). Thepresence of elevated divalent ions may beimportant in allowing the dreissenids to tol-erate more saline environments. The diva-lent cations are intimately involved in cellmembrane permeability and maintainingthe integrity of membrane junctional com-plexes (see Cereijido et al., 1983). After1980, the water of the Aral Sea becamemore saline and the dreissenid populationwas extirpated (Williams and Aladin,1991).

It is interesting to speculate on the evo-lutionary origin of the osmoregulatorystrategy utilized by D. polymorpha. Dreis-senids evolved in inland seas with a rela-tively constant or dampened salinity cycle(Morton, 1993). In a freshwater environ-ment, or one with a stable reduced salinity,organisms must reduce intracellular solutesto balance the reduction in blood solutes.The result is that K becomes the principalintracellular osmolyte. An advantage to uti-

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lizing K for intracellular volume regulationis that it would allow proper electrochemi-cal balance between the cells and body flu-ids. Freshwater animals have reduced theproportion of free amino acids (FAA) con-tributing to the pool of intracellular solutes(Hanson and Dietz, 1976; Gainey, 1978;Day et al., 1990; Matsushima and Hayashi,1992). Conversely, bivalves inhabitingbrackish water or environments with fluc-tuating salinity typically employ both FAAand K for intracellular volume regulation(Deaton et al, 1989; Silva and Wright,1994). The utilization of FAA as a substan-tial proportion of the total intracellular os-motic concentration may create an osmolytebuffer system allowing the animal to retaincell water in the face of dehydration in-duced by hyperosmotic conditions. Thisstrategy may have freed brackish water an-imals from a total reliance on K for volumeregulation. The inability of freshwater or-ganisms to accumulate modest to high FAAmay lead, in part, to their intolerance of hy-perosmotic stress. The inability of Dreis-sena, and perhaps other freshwater bi-valves, to tolerate hyperosmotically induceddehydration may be due, in part, to the lackof a significant intracellular FAA pool andthe inability to accumulate or retain suffi-cient intracellular K to prevent an excessivereduction in cellular volume.

ACKNOWLEDGMENTS

We thank S.J. Nichols for providingsome of the animals from Lake Erie and Dr.R. F. McMahon for many helpful sugges-tions and comments. T. R. LeBlanc at DowChemical, Plaquemine, LA, provided ani-mals from the Mississippi River. DiondiLessard, Tim Smith, Ron Bouchard, JulieCherry, and Janice Horohov provided tech-nical assistance. This work was supportedby NSF grant DCB90-17461 and LouisianaSea Grant NOAA 46RG00960 ProjectR/ZMM-1.

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Aladin, N. V., and W. T. W. Potts. 1992. Changes inthe Aral Sea ecosystem during the period 1960—1990. Hydrobiologia 237:67-79.

Cereijido, M., L. Gonzalez-Mariscal, and L. Borboa.1983. Occluding junctions and paracellular path-ways in monolayers of MDCK cells. J. Exp. Biol.106:205-215.

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Deaton, L. E., J. G. S. Derby, N. Subhedar, and M. J.Greenberg. 1989. Osmoregulation and salinitytolerance in two species of bivalve mollusc: Lim-noperna fortunei and Mytilopsis leucophaeta. J.Exp. Mar. Biol. Ecol. 133:67-79.

Dietz, T. H. 1979. Uptake of sodium and chloride byfreshwater mussels. Can. J. Zool. 57:156-160.

Dietz, T. H., D. Lessard, J. W. Lynn, and H. Silverman.1994. Osmoregulation in Dreissena polymorpha:The importance of Na, Cl, K and particularly Mg.Biol. Bull. 187:76-83.

Dietz, T. H., R. A. Byrne, J. W. Lynn, and H. Silver-man. 1995. Paracellular solute uptake by thefreshwater bivalve Dreissena polymorpha. Am. J.Physiol. 269:R3OO-R3O7.

Fisher, S. W., P. Stromberg, K. A. Bruner, and L. D.Boulet. 1991. Molluscicidal activity of potassiumto the zebra mussel Dreissena polymorpha: Tox-icity and mode of action. Aquatic Toxicol. 20:219-234.

Gainey, L. E, Jr. 1978. The response of the Corbicu-lidae (Mollusca: Bivalvia) to osmotic stress: Thecellular response. Physiol. Zool. 51:79—81.

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