Respiratory adjustment of dreissenid mussels (Dreissena polymorpha and Dreissena bugensis) in response to chronic turbidity

Abstract

A laboratory study was conducted to determine the effect of chronic turbidity (using bentonite clay) at medium and high temperatures on respiration of two exotic mussel species, Dreissena polymorpha and Dreissena bugensis. Populations of D. polymorpha from Lake Erie and the Ohio River and D. bugensis from Lake Erie were acclimated for 4 weeks to one of four temperatureñturbidity combinations: 25∞C ñ 0 nephelometric turbidity units (NTU), 25∞C ñ 80 NTU, 15∞C ñ 0 NTU, and 15∞C ñ 80 NTU. At the end of the acclimation period, respiration was measured at both 0 and 80 NTU using a closed, flow-through system with a Clark-type polarographic microelectrode. Mass-specific respiration rates were computed as V · O2 ( =μ L O2 consumed·mg shell-free dry massñ1·hñ1). Results showed that size, temperature, acclimation turbidity, and measurement turbidity significantly affected V · O2 rates. An interaction between acclimation turbidity and measurement turbidity suggests that dreissenid mussels adjusted their metabolic rate in response to chronic exposure to turbidity. Mussels acclimated to higher levels (80 NTU) of turbidity did not experience as large a percent drop in V · O2 when tested in turbid water

Full text

Respiratory adjustment of dreissenid mussels
(Dreissena polymorpha and Dreissena bugensis)
in response to chronic turbidity
R.BrentSummers, JamesH. Thorp, JamesE. Alexander,Jr.,and RonaldD. Fell
Abstract: Alaboratorystudywas conducted to determinetheeffect of chronicturbidity (using bentoniteclay)at medium and
high temperatures on respiration of two exotic mussel species, Dreissena polymorpha and Dreissena bugensis.Populations of
D.polymorpha fromLake Erie and the OhioRiver and D.bugensis fromLake Erie wereacclimated for 4 weeks to one of
four temperature–turbiditycombinations: 25°C – 0 nephelometricturbidity units (NTU), 25°C – 80 NTU, 15°C– 0 NTU,and
15°C– 80 NTU. At the end of theacclimation period, respiration was measured at both 0 and 80 NTUusing aclosed,
flow-through systemwith aClark-type polarographic microelectrode. Mass-specific respiration rates were computed as V
⋅O2
(=µLO2consumed⋅mgshell-freedry mass–1⋅h–1). Results showed that size, temperature, acclimation turbidity, and
measurement turbidity significantlyaffected V
⋅O2rates.An interaction betweenacclimationturbidity and measurement
turbiditysuggests that dreissenid mussels adjusted their metabolic rate in response to chronic exposure to turbidity. Mussels
acclimated to higherlevels (80 NTU) of turbiditydidnot experience as largeapercent dropin V
⋅O2when tested in turbid water
(80 NTU) as did musselsacclimated at lower turbidity (0 NTU).
Résumé : Nous avons menéune étudeen laboratoire pour déterminer l’effet dela turbidité chronique (à l’aide d’argile
bentonitique)à des températures moyennes et élevées sur la respiration de deux espèces de mollusquesexotiques, Dreissena
polymorpha et Dreissenabugensis. Les populations de D.polymorpha du lac Érié et du fleuveOhio et de D.bugensis du lac
Érié ont été acclimatées pendant 4semaines avecl’une des quatrecombinaisons suivantes de température et turbidité: 25°C –
0unités deturbiditénéphélémétriques (UTN), 25°C – 80 UTN, 15°C– 0 UTNet 15°C – 80 UTN.Àla fin de la période
d’acclimatement, on a mesuré la respiration à0 et à80 UTN àl’aide d’un systèmeferméencirculation avecune
microélectrodepolarographiquede type Clark. Onacalculé les tauxde respiration spécifiques dela masse sous la forme V
⋅O2
(=µLO2consommé⋅mgmasse sèche sans coquille–1⋅h–1). Les résultats ont montré que la taille,la température, la turbidité
d’acclimatement et la turbidité à la mesure avaient des effets significatifs surles taux de V
⋅O2.Une interaction entrela turbidité
d’acclimatement et la turbidité à la mesure permet depenser que les dreissenidés ont adaptéleur taux métaboliqueen réaction
àune exposition chronique àla turbidité. Les moules acclimatées àdes niveaux supérieurs (80 UTN) de turbidité n’ont pas
connu une baisse aussi forteenpourcentagede V
⋅O2lorsqu’on les atestées dans une eau trouble(80 UTN) que les moules
acclimatées àune turbidité plus faible(0 UTN).
[Traduit par la Rédaction]
Introduction
The spread of the zebra mussel (Dreissena polymorpha Pallas)
and quagga mussel (Dreissena bugensis Andrusov) throughout
eastern North America has been well documented since their
initial colonization in the Great Lakes in 1986 (Hebert et al.
1989) and the former’s rapid spread into the Mississippi and
Ohio rivers. Zebra and quagga mussels are expected to dis-
perse throughout much of the remainder of the central and
eastern parts of the United States and the southern portion of
Canada (Strayer 1991).Zebra musselscurrently inhabitmany
largeriver systems east of the RockyMountains including the
St. Lawrence,Hudson, Mississippi, Tennessee, Arkansas, and
Ohio rivers. The quagga mussel is presently restricted to the
lower Great Lakes and the St. Lawrence River (New York Sea
Grant 1994; Mills et al. 1993); however, isolated individuals
have been collected in the Mississippi River near St. Louis,
Missouri. The quagga mussel is expected to spread throughout
most of the range currently occupied by zebra mussels. The
quagga mussel may also occupy profundal areas of lakes that
are not exploited as well by zebra mussels,thus posing a new
problemto native, deep water assemblages in these lentic eco-
systems(Millsetal. 1993).
Dreissenid mussels in large rivers face a much different
challenge in terms of both biotic and abiotic factors than do
lake populations (for a review of relevant differences between
lakes and large rivers, see Strayer 1991; Thorp et al. 1994). As
dreissenid mussels have colonized southward from the Great
Lakes into rivers, they have encountered increased turbulence,
temperatures, and sediment loads (Alexander et al. 1994), as
well asother differences inchemical, physical, andbiological
characteristics.
One important disparate factor that plagues dreissenid mus-
sels in large river systems is the higher levels of suspended
inorganic sediment (turbidity). Inorganic turbidity presents a
wide range of problems for aquatic animals, particularly
Received October18, 1995.Accepted February15, 1996
J13117
R.B.Summers, J.H. Thorp,1and J.E. Alexander, Jr. Large
River Program,BiologyDepartment, Universityof Louisville,
Louisville,KY 40292,U.S.A.
R.D. Fell. BiologyDepartment, Universityof Louisville,
Louisville,KY 40292,U.S.A.
1Author to whomall correspondenceshould be addressed.
e-mail: jhthor01@ulkyvm.louisville.edu
Can. J. Fish. Aquat. Sci. 53: 1626–1631 (1996).
1626
© 1996NRC Canada

filter-feeding organisms (Wilbur 1983). The deleterious ef-
fects of inorganic turbidity on suspension-feeding bivalves in-
clude fouled gill tissues, increased pseudofecal production
(Widdows et al. 1979; Bricelj and Malouf 1984), reduced
feeding efficiency (Bricelj et al. 1984), and interference with
respiratory surfaces (Morton 1971; Aldridge et al. 1987;
McMahon 1991). Collectively, these effects impose larger
costs on the energy budget of suspension-feeding bivalves.
Studies by Alexander et al. (1994) examining acute effects of
temperature and turbidity on D. polymorpha showed that res-
piration decreased with increasing turbidity up to 80 NTU
(equivalentto 500 mgsediment/L), after which higher experi-
mental concentrations did nothave asignificantly more nega-
tive effect on respiration. Respiratory rates rose with
increasing temperatures (Q10(acc) =1.96), as is commonly seen
for ectothermic animals (McMahon 1991; Alexander et al.
1994). Although riverine populations of mussels are exposed
to acute bursts of inorganic turbidity as a result of short but
often severe storm events (Alexander et al. 1994), they also
face higher chroniclevels of turbidity for a significant portion
of the year in large rivers such as the Ohio (Fig. 1).
The primary goal of this study was to evaluate how chronic
exposure to inorganic turbidity at medium and high tempera-
tures affects the two species of Dreissena currently known
present in North America. We hypothesized that the chronic
effects of these two variables would differ from the acute re-
sponses, with D. polymorpha or D. bugensis adjusting their
respiratory rates in response to changes in temperature and (or)
turbidity. This prediction of physiological adjustment is based
in part on findings of Way et al. (1990), who showed that the
Asiatic clam Corbicula fluminea alters its physiology in re-
sponse to changing environmental conditions (e.g., variable
turbidity), thus maintaining optimal filtering rates. An impor-
tant applied goal of this study was to contribute information
that will help predict the success of these two mussels in the
rivers of North America.
Materials and methods
Experimental design and maintenance
The effects of temperature and chronic exposure to suspended sedi-
ments (=turbidity) on mussel respiration were determined in a 3 ×2×
2 experimental design. Three populations of mussels (D. polymorpha
from Lake Erie and the Ohio River, and D.bugensis fromLake Erie)
wereobtained forthe experiment. Two lentic samples of both D.po-
lymorpha and D. bugensis were collected by scuba divers from San-
dusky Bay (western Lake Erie) from 7 m depth in the fall of 1993 and
summer of 1994. Samples of D.polymorpha were collected fromthe
population in the Ohio River near Louisville, Kentucky, during the
fall of 1993 and the spring and summer of 1994, by removing mussels
from rocks in theshallow littoral zone.
Upon collection, mussels were immediately transported to the
laboratory where they were sorted into size-classes of 4 mm length,
placed in an environmental chamber, and acclimated to one of four
combinations of temperature and turbidity under a 12 h light : 12 h
dark photoperiod. Replicatesamples (N=16 for each treatment con-
dition) of each population were acclimated for at least 4 weeks to one
of four temperature–turbidity conditions: 15°C – 0 nephelometric tur-
bidity units (NTU), 15°C – 80 NTU, 25°C – 0 NTU, or 25°C –
80 NTU. Temperatures in the chambers were adjusted to the acclima-
tion level at a rate of 1°C/day, and then kept at 15 or 25°C for at least
4 weeks. Turbidity levels were maintained at 0 and 80 NTU by adding
bentonite clay to U.S. Environmental Protection Agency standard
freshwater (hard type; APHA 1985) in 3-L animal-holding containers
that were continuously and vigorously aerated to maintain the clay in
suspension. One gram per litre of bentonite clay used in this study was
equal to 660 NTU. Turbidity levels were measureddaily with a Hach
turbidimeter (model 2100p) and adjusted as required. This 4-week
temperature and turbidity acclimation period was sufficiently long to
allow any physiological, morphological, or behavioral changes to
take place as a function of the temperatureor turbidity treatment.The
temperature and turbidity levels were chosen on the basis of recent
patterns of these two factors in the Ohio River. The overall inverse
pattern of mean monthly temperatures and turbidity levelsin the Ohio
River fora 14-year period(1981–1994)is showninFig. 1. This pre-
sumably noncausal but significantlycorrelated relationship(R2=
–0.975) is based on other seasonal abiotic factors such as precipitation
patterns and river discharge (Alexander et al. 1994). Temperatures
usually ranged from 3°C (January) to 27°C (August), while turbidities
varied from 4 NTU during low flow periods to 80 NTU during high
flowintervals.
While in the acclimation chamber, mussels were kept in 2-mm
mesh bags within the 3-L containers and fed live Chlorella vulgaris
every2 days, withtheir water completely changed every 3 days. The
number of mussels per bag depended on the size-class ofmussels. For
example, 20 mussels 6.0–10.0 mm long were added to a bag, whereas
only 5 mussels 25.0–30.0 mm long were used. The mussels were then
placed in 3.5-L plastic containers containing 3.0 L of U.S. Environ-
mental Protection Agency standard freshwater (hard type; APHA
1985). The potentiallyconfounding effect of body mass was control-
led by using five size-classes within each treatment level for a total of
16 replicates per acclimation condition. The size-classes and replicate
numbers were 6.1–10.0 mm (N=3), 10.1–15.0 mm (N=3),
15.1–20.0 mm (N=4), 20.1–25.0 mm (N=3), and 25.1–30 mm
(N=3).
Measurement of respiration
An experimental run consisted of four steps: (i) a 5-min habituation
periodwith mussels in clear water (0 NTU), (ii) a 20-min measurement
Fig. 1. Monthly meantemperatures (open squares and solid line)
and turbidity levels (solid circles and brokenline) for a14-year
period (1981–1994) in the Ohio River near Louisville, Kentucky
(datacollected by the LouisvilleWater Company’s Byron E.Payne
water treatment plant). Errorbars arestandard errors of themeans.
Summers et al. 1627
© 1996NRC Canada

period at 0 NTU, (iii) a second 5-min habituation period during which
the mussels were exposed to the second test turbidity of 80 NTU, and
(iv) a second 20-min measurement period at80 NTU. The habituation
periods provided ample time for mussels to open their valves, extend
their siphons, and begin filtering (cf. Alexander et al. 1994). During
habituation and measurement periods, mussels were held in a cylin-
drical, glass respiratory chamber (9 cm long and 2.5 cm inner diame-
ter). Holed rubber stoppers were placed at each end with stopcocks to
control water flow through the clear chamber. All water was cooled
or heated to the proper temperature and aerated to ensure full oxygen
saturation (partial pressure of oxygen was 20.53–20.93 kPa). A per-
fusion pump (Gilson minipuls perfusion pump, model 312) propelled
waterin a completecircuit through perfusiontubes, in and out of the
respiratory chamber, and past the oxygenelectrodeat 20mL/min. A
Cole-Parmer perfusion pump (model 7520) circulated water from a
water bath through a water jacket and around a YSI oxygen mi-
croelectrode (calibrated before each series of tests) to maintain it at
the proper test temperature. The continuous pumping of water
throughthesystem adequately maintained turbidity levels inthe res-
piratory chamber. Oxygen levels were measured with a YSI oxygen
meter (model 5300). The data were acquired using an analog to digital
converter with a MacIntosh computer and Acknowledge (version 2.1)
data acquisition software.
Shell-free, dry tissue masses were determined using the proce-
dures outlined by McMahon (1985) and Alexander et al. (1994). After
a group of animals was tested, they were dried in an oven at 85°C for
several days until a constant mass was achieved. The dried tissue,
which was easily removed from the shell (mantle tissue in some cases
was easily removed from the inner shell wall by gently scraping), was
weighed using a Cahn microbalance (model C-33). Shell-free dry
biomass values were employed to calculate mass-specific oxygen
consumption rates (V
⋅O2=µLO
2consumed⋅mg shell-free dry
mass–1⋅h–1).
Statistical analyses
A normality test of the data showed no significant departure from a
normal distribution; therefore, parametric procedures were employed
for analyses using the Statistical Analysis System(SAS Institute Inc.
1990). Owingto a slightlyunbalanced experimental design(unequal
replicate numbers among all size-classes), a general linear models
(GLM) procedure was usedto perform analysis of variance. The ex-
periment involved both a nested and split plot design (each replicate
group measuredat both 0 and 80NTU). A split plot designwasutil-
ized owing to the repeated measure of respiration at both 0 and
80 NTU on the same group of animals. Main treatment effects of
species, temperature, acclimation turbidity, and sizewere determined
using the data independent of measurement turbidity, while effects
relating to measurement turbidity (interactions of measurement tur-
bidity with species, temperature,acclimation turbidity, and size) were
determined separately. Expected mean squares for hypothesis tests
were determined according to rules given by Damon and Harvey
(1987) and used to determine appropriate error terms for tests of
hypothesis (see Table 1 for mean square values and error terms).
Tukey’s studentized range (honestly significant difference, HSD)
tests were used to perform multiple comparisons where appropriate.
An alpha level of p≤0.05was used to indicatesignificance of tests.
Results
Temperature and turbidityeffects on respiration
Animals acclimated and measured at 25°C had significantly
higher V
⋅O2rates than those at 15°C (Fig. 2; Table 1), as is
commonly seen for ectothermic animals. In general,V
⋅O2rates
dropped 25–50% (Fig. 2; Table 2) in turbid water, depending
ontemperatureand acclimationturbidity. Mussels acclimated
at0NTU and tested at0 and 80 NTU showed a larger percent
drop in V
⋅O2than mussels acclimated at 80 NTU under identical
test conditions (Fig. 2; Table2). Therewas a significant inter-
action of temperature with measurement turbidity (Table 1),
which indicates that musselsacclimated at 25°Chadagreater
depression of respiratory rate when tested under turbid condi-
tions(80 NTU) than mussels acclimated at15°C.
Size and species effects on respiration
Size had a significant effect on respiration (Table 1), with
smaller mussels having relatively higher V
⋅O2rates (recall that
Sourceof variation df MS Fp
Populationa2 0.57 17.26 0.0001
Temperaturea1 5.86 176.47 0.0001
Sizea4 0.09 2.75 0.0001
Measurementturbidityb1 26.42 982.69 0.0001
Species ×measurement turbidityb2 0.06 2.40 0.0944
Temperature ×measurment
turbidityb
1 0.29 10.65 0.0014
Size ×measurement turbidityb4 0.12 4.52 0.0018
Acclimation turbidity ×
measurement turbidityb
1 0.78 29.00 0.0001
Note: All othersecond and higherorder interactions arenonsignificant
(α=0.05).
aError term =group (species ×temperature ×acclimation turbidity ×size).
bError term =measurement turbidity ×group (species ×temperature ×
acclimation turbidity ×size).
Table1. General linearmodel analysis of varianceresults. Fig. 2. Respiratoryresponses (V
⋅O2=µLO2⋅mg–1⋅h–1)of the zebra
mussel (LEZ) and quagga mussel (LEQ) from LakeErie,and the
zebra mussel (ORZ) fromtheOhio River. Mussels were acclimated
for 4 weeks to one of four temperature–turbiditycombinations:
25°C –0 NTU(solid circles), 25°C – 80 NTU(solidsquares),
15°C –0 NTU(opencircles), and 15°C –80 NTU (open squares).
Respiration wasmeasured at both0 and 80 NTU. Error bars are
standard errors of the mean(N=16) for each acclimation condition.
Can. J. Fish. Aquat. Sci. Vol. 53, 1996
1628
© 1996NRC Canada

V
⋅O2is a mass-adjusted parameter).Nosignificant interactions
occurred between size and species, size and temperature, and
size and acclimation turbidity in terms of respiration (Table 1).
These nonsignificant interactions suggest that respiratory rates
for the three populations responded similarlyamong size-
classes, regardless of the acclimation temperature and turbid-
ity. In contrast,V
⋅O2rateswere influenced bya significant
interaction between measurement turbidityand size (Table 1).
Consequently, smaller Dreissena spp. had a larger percent
drop in V
⋅O2than larger mussels when they were exposed to
turbidconditions immediately aftertestinginclear water.
Although respiration differed between populations
(Table 1), the two species (includingbothpopulations of
D. polymorpha) reacted in the same way to turbidity, tempera-
ture, acclimation turbidity, and size (Table 1). This indicates
that although populations of D. polymorpha and D. bugensis
had different respiratory rates, they all had the same functional
response to temperature, acclimation turbidity, and size. The
species difference in respiratory rate is not clear because the
two populations of D. polymorpha (Lake Erie and Ohio River)
were split into separate species–location groups for the pur-
pose of analyzing population differences. Using a Tukey’s
range (HSD) multiple comparisons test, no significant differ-
ences were present between the two populations of zebra mus-
sels (Lake Erie and Ohio River) or between Lake Erie zebra
and quagga mussels. Therewas, however, a significant differ-
ence between Ohio River zebra mussels and Lake Erie quagga
mussels. All higher order interactions relative to size or spe-
cies–location group were nonsignificant (p < 0.05).
Acclimatory effect of turbidity
A significant interaction existed between acclimation turbidity
and test turbidity (Table 1). As shown in Fig. 2, mussels accli-
matedat 0 NTU had higher V
⋅O2rates thanmussels acclimated
at 80 NTU when tested in clear water. However, when the
musselsweretested inturbid water, the mussels acclimatedat
80 NTU had higher rates than those acclimated at 0 NTU. The
mussels acclimated at 0 NTU showed a significantly larger
percent drop in V
⋅O2rate than did mussels acclimated at
80 NTU (Table 2). This interaction, as evident fromthe cross-
ing of lines in each of the different temperature groups in
Fig. 2, suggests that some form of adjustment to suspended
sediment occurred during the 4-week acclimation phase of the
experiment.
Discussion
Metabolic turbidity acclimation
Turbidity effects on growth, filter feeding, and to a lesser ex-
tent respiration have been widely studied in both marine and
freshwater bivalve molluscs (Foster-Smith 1975; Winter 1978;
Widdows et al. 1979; Kiorboe et al. 1981; Bricelj et al. 1984;
Bricelj and Malouf 1984; Foe and Knight 1985; Aldridge et al.
1987; Way et al. 1990; McMahon 1991), including a few stud-
ies conducted on dreissenid mussels (Morton 1971; Sprung
and Rose 1988; Reeders and Bij de Vaate 1990; Wisniewski
1990; Quigley et al. 1993; Alexander et al. 1994; Payne et al.
1995). The effects of turbidity on clams and mussels vary con-
siderably with the sediment particle size and composition,
level of turbidity, and temperatures used in the experiment
(Payne et al. 1995). One effect of turbidity on bivalves is a
depression of respiratory rate. In some marine and freshwater
bivalves, normal levels of turbidity have moderate to relatively
little effect on respiration (Widdows et al. 1979; Aldridge et al.
1987). In contrast, a study by Alexander et al. (1994) showed
that respiration in the freshwater mussel D. polymorpha was
depressed when this mollusc was exposed to relatively low
levels (5 NTU) of acute turbidity, thus suggesting that dreis-
senid mussels may be more sensitive to suspended sediment
than other tested marine and freshwater bivalve molluscs. The
mechanism causing a drop in respiration with increasing tur-
bidity is unclear. Suspended solids may overload the gut and
gills (Morton 1971) or physically impede water currents or gas
exchange across gill membranes (Aldridge et al. 1987; McMa-
hon1991).
The results of this study suggest that D. polymorpha and
D. bugensis can partially acclimate to turbid water conditions
by adjusting their metabolic rate. This occurs when mussels
are allowed to acclimate at a moderate to high level of chronic
turbidity (80 NTU bentonite clay) for an extended period
(4 weeks). It appears that mussels acclimated to chronic tur-
bidity maintain a more constant metabolic rate over a range of
turbidities than mussels that have not been acclimated to turbid
conditions, as evidenced by a comparison of the animals ac-
climated at 0 and 80 NTU within a temperature group when
they were tested in turbid water (Fig. 2; Table 2). The mussels
acclimated at 80 NTU did not experience as large a percent
drop in V
⋅O2as did the mussels acclimated at 0 NTU (Fig. 2;
Table 2).
The factor responsible for this acclimation has not been
specifically identified, but it should be either a physical, bio-
chemical, behavioral, or combined mechanism. A behavioral
change might be elicited by mussels conditioned to an envi-
ronmental stimulus, such as turbidity; however, preliminary
studies in our laboratory (R.B. Summers, J.H.Thorp, J.E.Al-
exander, Jr., and R.D. Fell, unpublished data) indicated that
mussels acclimated to 80 NTU turbidity show no difference in
the percent time with their valves open and filtering under
different levels of turbidity (0 and 80 NTU). Biochemical
changes are common for bivalves in response to a range of
environmental factors (McMahon 1991). Biochemical compo-
nents that may affect respiration include changes in aerobic
metabolic pathways, enzyme level and activity, hemolymph
and blood chemistry, substrate oxygenaffinity, andgillmem-
brane conformations (fluidity). A physical alteration may be
Species and acclimation
temperature (°C)
Acclimation turbidity (NTU)
080
15 LEZ 43.8±0.8 32.9±1.2
25 LEZ 38.1±1.0 31.1±1.2
15 LEQ 45.2±2.2 35.3±2.5
25 LEQ 52.4±1.8 27.8±4.5
15 ORZ 39.4±4.4 25.1±4.5
25 ORZ 35.5±2.8 28.6±1.8
Note: Values represent the mean (±1 SE) percent decrease in V
⋅O2for
each species ×acclimation condition measured firstin clearwater (0 NTU),
and then in turbid water(80 NTU).
Table2. Percent decrease in respiratoryrate (V
⋅O2)for each
population or species(Lake Erie zebra mussels, LEZ; LakeErie
quaggamussels, LEQ; and Ohio river zebra mussels, ORZ)and
acclimation condition (15 or 25°C; 0 or 80 NTU).
Summers et al. 1629
© 1996NRC Canada

expressed as a modification in gill surface area,change in the
structure or function of gill cilia, or a combination of factors
influencing filtration and respiration rates. Physical changes
such as these have been shown to occur in bivalves on both
acclimatoryand developmental levels. A study by Payne et al.
(1995) showed that ecophenotypic differences existed within
populationsof both D. polymorpha and the Asiatic clam Cor-
bicula fluminea, in which populations in habitats characterized
by relatively high suspended sediments showed a marked in-
crease in labial palp to gill area ratios. The increase in labial
palp size and decrease in gill size (in C. fluminea) is apparently
adaptive in the presence of high concentrations of suspended
solids.Enlargedpalp size increasesthe particle sortingability
of the mussels, thus allowing higher clearance and ingestion
rates (Payne et al. 1995). A similar study byWayet al. (1990)
demonstrated that C. fluminea makes physiological adjust-
ments in response to certain environmental conditions (e.g.,
suspended sediment), thereby maintaining optimal filtration
rates.
It is known that without time for acclimation, mussels typi-
cally reduce their clearance rate (volume of water passing
through gills per unit time), thus potentially lowering their
intake of oxygen and food (Aldridge et al. 1987). With a suf-
ficient period for adjustment, mussels may acclimate to turbid-
ity by more effectively rejecting certain particles
(e.g., inorganic material). This in turn would result in higher
pseudofecal production, clearance rates (without overloading
the filter-feeding apparatus), and ingestion rates (B.S. Payne,
Environmental Laboratory, U.S. Army Engineer Waterways
Experiment Station, Vicksburg, MS 39180, U.S.A., personal
communication). Increases in pseudofecal production, clear-
ance rate, and ingestion require greater energy expenditures
and increased oxygen consumption. This type of acclimation
appears to be the most plausible explanation of our results;
however, further experimentation is necessary to determine the
exact physiological basis of our findings.
The adaptation to turbidity shown here suggests that zebra
and quagga mussels will be able to colonize turbid lakes and
rivers at higher densities than was previously thought (see
Strayer 1991). This is supported by the presence of the zebra
mussel, and to a lesser extent the quagga mussel, in several
river systems of North America, where substantial densities
have been achieved (e.g., < 20000 mussels/m2in the Ohio
River). Our data indicate that the effect of turbidity on respi-
ration, and possibly growth and reproduction, will not be as
dramatic aspreviously reported. Wepredict thatzebra mussel
densities will not be unduly limited by the temperature range
(4–30°C) and chronic turbidity levels (0–100 NTU) normally
encountered in large floodplain rivers such as the Ohio and
Mississippi. However, in extremely turbidrivers (chronic val-
ues < 150 NTU) mussels may be overwhelmed by the large
amountofsuspendedand deposited sediments, thus com-
pounding the previously mentioned problems associated with
turbidity. Under these conditions of extreme chronic turbidity,
dreissenid mussels may either exist at lower densities or never
establish viable populations. This may be the case in an ex-
tremely turbid river such as the Missouri (Ellis et al. 1937;
Pflieger and Grace 1987), which has had ample opportunities
for colonization through commercial barge traffic (the primary
upstream dispersal vector),but which currently lacks a viable
zebra mussel population (Zebra Mussel Information Clearing-
house, Brockport, N.Y., April 1995). It is unclear if this lack
of colonization can be attributed entirely to high inorganic
turbidity in the Missouri River or to some other factor, such as
naturally high potassium levels.
Acknowledgements
The authors thank Andy Casper, KurtBresko, Kim Haag,and
Tim Sellers for various aspects of the research,
Dr. Gary Cobbs for statistical advice, and Dr. Barry S. Payne
for comments on the physiological basis of the findings. The
authors also appreciate the aid of Heather Middleton in organ-
izing Ohio River temperature and turbidity data provided by
the Louisville Water Company. This research was supported
by a cooperative agreement from the U.S. Environmental Pro-
tection Agency (CR820263–01–0 to J.H.T.) and a contract
from theAmerican WaterWorks AssociationResearch Foun-
dation (733–91to J.H.T.).
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