Effects of Hypoxia and Low-Frequency Agitation on Byssogenesis in the Freshwater Mussel Dreissena polymorpha (Pallas)

8 Pages·1996·3.2 MB·English

by  M Clarke

Reference: Bio/. Bull 191:413-420.(December, 19%)
Effects of Hypoxia and Low-Frequency Agitation on
Byssogenesis in the Freshwater Mussel
Dreissena polymorpha (Pallas)
MICHAEL CLARKE AND ROBERT McMAHON
F.
Department ofBiology, UniversityofTexasatArlington, Box 19498, Arlington, Texas, 76019-0498
Abstract. The effect ofvariations in Po2 and agitation damaging macrofouling pest species in North America
rate on byssogenesis, motility, and survival ofthe zebra and Europe (Mackie et a/., 1989; Claudi and Mackie,
mussel (Driessena polymorpha) was investigated. Mus- 1993).
sels exposed to a Po2 < 15.4torr exhibited increased Several environmental factors influence the rate of
mortality, reduced motility, and significant suppression byssogenesis in marine byssate mussels such as Mytilus
of byssogenesis. At 7.7 and 15.4torr, mean survival edulis L., Geukensia demissus (Dillwyn), and Perna in-
times were 5.2 and 5.8 days, maximum survival times dica Kariakose and Nair. These include temperature
being 15 and 16 days, respectively. After21 daysataPo2 (van Winkle, 1970), current velocity (Lee et al, 1989),
of23.1 torr, samplemortalitywas 33.3%anddeclinedto ambientoxygenconcentration(Ravera, 1950; Reishand
O
18.2% at 30.9 torr. There was no mortality at full air 2 Ayers, 1968), agitation rate (van Winkle, 1970; Young,
saturation (~154.3 torr). Adult zebra mussels exhibited 1985), salinity (Young, 1985; Mathew and Fernandez,
thehighestrateofbyssogenesisin still water(0 cyclesper 1992), and seasonal variations in abiotic factors (Price.
minute [CPM]). Rate ofbyssogenesis progressively de- 1980, 1982). Changes in a mussel's ability to produce
creased as agitation rate increased. At 30 and 40 CPM, byssalthreadscan havefar-reachingconsequences;wave
rate ofbyssal thread production was significantly lower action and tidal rhythms continually subject intertidal
than at CPM. After 21 days, means of 58.6 and 44.8 inhabitants to strong mechanical forces, and high levels
byssal threads/mussel were found in the byssal mass of ofmortality occurwhen mussels becomedetached from
specimens exposed to 30 and 40 CPM, respectively, sig- thesubstratum (Hargerand Landenberger, 1971).
nificantlyfewerthanthemeanof92.7 threads/musselre- There is wide taxonomic separation between mytilid
corded in still water. Suppression ofbyssogenesis in D. and dreissinid bivalves. They also have different evolu-
polymorphaunderhypoxicconditions isa responsesim- tionary histories, one evolving in high-energy intertidal
ilartothatreportedforthemarinemytilidMytiliseditlis; marine habitats, the otherin low-energy freshwater hab-
however, suppression ofbyssogenesis with elevated agi- itats. Their contrasting evolutionary histories may have
tation rate is the opposite response to that reported for resulted in differencesin howthephysiological processes
M. edulis. thatregulatetherateofbyssogenesisrespondtochanging
environmental conditions (Clarke and McMahon,
Introduction 1996a).
The zebra mussel, Dreissena polymorpha (Pallas Theeffectsofcurrent velocityand temperatureon the
c1u7r7e1t),oahafrredsshuwraftaecresbi(vMaolvretomno,ll1u9s6c9,).usTehseacboymsbsuisnattoisoen- qrautaentoiffizeedbraanmduscsoemlpbayrsesdogetonestihse hraevsepobneseesn porfevmiaoruisnley
ofa highly dispersive larval stage and retention of the mytilids(Clarke and McMahon, 1996b, c). In this paper
byssal holdfast as an adult has made the zebra mussel a we investigate the effects ofhypoxia and low-frequency
agitation on byssal thread production by D. polymorpha
and compare the results to data published for mytilid
Received 19April 1996;accepted25September 1996. species.
413
414 M. CLARKE AND R. F. McMAHON
Materialsand Methods berin the rotation foran equivalent time period. Conse-
quently, each mussel was exposed equally to any "tank
Specimen collectionandmaintenance
effect" that may have been associated with a particular
Specimens ofD. po/ymorp/ui were collected from the chamber in the rotation. This allowed each individual
upstreamguidewall ofBlack Rock Lock, on the Niagara mussel to be treated as an independent, or "true," repli-
River, Buffalo, New York. They were transported over- cate in the statistical analysis.
night to The University ofTexasat Arlington and main- Mean shell length (SL) thegreatest lineardimension
tained in aerated, dechlorinated tap water in a 280-1 from the tip ofthe umbos to the posterior margin ofthe
t"unaLtiiinvleidnugsuenSddterirnetaehmxe"pseehrcoiolmndedinitntsgi.otnaSsnpkewicatithm5elinCtst,lehwmaiovtrehtoabuleitetnyfeoemrdailinongs-,s (s1h27e..l8l7,mmnof=(t3h2.e8)2maSutDs,s15e/.l;4s=tou2rs8re);da1t5f.Po3rom2em=ach7(.27.ttr4oe,rar;tnm1e=5n.t428m)wamast
of tissue mass for over 1 year (Chase and McMahon, 23.1 mtomrr; 17.4m=m (2.9, /; = 28) at 30.9 torr and
1994). Specimens ofD. bugensisin the sample were vis- 16.6 (2.6, // 48)at 154.3 torr.
ually identified according to descriptions by May and The cumulative number of new byssal threads pro-
Marsden (1992) and removed. All specimens were used duced by reattaching mussels was recorded daily for
within 60daysofcollection. 21 daysaftertheinitial reattachment(day 0). Newbyssal
threads were counted by viewing the underside of the
mussel, through the clear plastic plate, on a dissection
Responsestohypoxia
microscope at 45X. Sites of thread attachment to the
Prior to experimentation, mussels were acclimated in plate (i.e.. the plaques) were clearly visible when viewed
17 1 ofaerated dechlorinated waterto a test temperature in this manner. Thelocationofnewplaqueswasmarked
of25C for2 weeks. Duringacclimation, constant water each dayon the undersideoftheplatewitha fine-tipped,
temperature (1C) was maintained by holding aquaria waterproof, permanent ink marker. This procedure al-
in incubators. After acclimation, the byssus of experi- lowed quantitative determination ofthe effectsofdiffer-
mental mussels was severed at the byssal gape with a ra- entPo2levelson byssal thread production. Timetomor-
zor blade. Immediately after byssus removal, mussels tality ofindividual mussels in the samples was recorded
were placed on clear plastic plates (14 X 14 X 0.2 cm) daily, as was time of any relocation of mussels on the
located in the bottom of 17-1 aquaria. Mussels were al- plastic plates (detachment from the byssus followed by
lowed to byssally reattach to the plastic plates for 12 h. relocation and reattachment is common behavior
The range of byssal thread production by individuals amongadultsofthisspecies, Mackie rt ai. 1989).
duringthe 12-h reattachmentperiodwas4to26 threads/ The resulting data were tested for statistical signifi-
mussel. cance by analysis of covariance (ANCOVA) in which
Followingthe reattachment period, each plastic plate, Po2 level was the main treatment, days was a repeated
togetherwitheitherfiveorsix attached mussels, wassub- measure, and mussel SL and number ofbyssal threads
mersed in 4 1 ofdechlorinated tap water held in individ- presentatday werecovariates. The null hypothesisthat
ual 5-1 capped plasticchambers(22 X 22 X 12 cm) leav- variationsin oxygen partial pressure had noeffecton the
ing 1 1 ofgas head-space. Water in these chambers was rate ofbyssal thread production was tested. A least sig-
continuously bubbled with mixtures ofoxygen and ni- nificantdifference(LSD)testwasemployedtodetectany
trogen gas. A Cameron GF-3 gas-mixing flowmeter reg- significant differences in rates ofbyssal thread produc-
ulated thegas mixtureto maintain median dissolved ox- tion between experimental Po2 levels.
O
ygen partial pressures(Po2)of7.7 torr(5% air 2 satura-
t(i1o5n%atai2r5OC:),sat1u5r.a4titoonr)r,(3100.%9atiorrrO(:2s0a%tuariartiOon:)s,at2u3r.a1titoonr)r Responses tolow-frequencyagitation
or 154.3 torr (100% air O2 saturation). Media Po2 was Specimens of D. po/ymorp/ia were acclimated and
measured daily with a polarographic silver-platinum ox- their byssus removed as previously described. Immedi-
ygen electrode(YSI Model 53). Chambermediawerere- atelyafterremoval ofthebyssus, musselswereplaced on
placedevery 2 days. ThePo2 offresh medium wasequil- clear plastic plates (7 x 7 X 0.2 cm) and allowed to by-
ibrated to the experimental levels by perfusion with the ssally reattach for 12 h. The number of byssal threads
appropriategasmixturefor24 hbeforemedium replace- produced by individuals during this period was 2 to 23
ment. threads/mussel.
Six chambers were used for each Po2 treatment level, The plastic plate and attached mussel were then se-
and the plastic plates were rotated among chambers cured with a stainlesssteel springclip to a fixed horizon-
daily.Thisrotationofspecimensthroughtheexperimen- tal stage, supported from aboveandsubmergedin 15 1of
tal chambers exposed individual mussels to each cham- dechlorinated tap water in a 17-1 plastic aquarium. The
ZEBRA MUSSEL BYSSOGENESIS 415
100 was temporally separated to prevent pseudoreplication
within treatments. The cumulative number of byssal
threads produced by reattaching mussels exposed to
varying agitation rates was recorded daily as previously
described for specimens exposed to hypoxic conditions.
Mussels were fed each day with rehydrated, washed,
freeze-dried green algae, Chlorella sp., in recommended
quantities (0.0032 g/mussel/day, Nichols, 1993). Me-
dium wasreplaced every 2 days.
Before completion ofthe 21-dayexperimental period,
some musselsspontaneously released from thebyssusor
were dislodged from their byssal hold-fasts by frictional
forces caused by water movements. These individuals
10 12 14 16 18 20 werenotincludedinthecalculation ofmeandailybyssal
Days thread production. Rates of byssal thread production
mm
were calculated for mussels with mean SL of21.9
(4.1 SD, n = 20) at CPM; 17.0 mm (2.1, n = 20) at
10 CPM; 17.2 mm (2.4, n = 20) at 15 CPM; 16.3mm
60 (3.0, n = 20) at 30 CPM; and 16.4 mm (3.1, n = 10)
1b at40 CPM.
50 Resultswere analyzed usinga repeated measuresAN-
^ COVA. Agitation rate was the main treatment effect;
40 mussel SLand numberofbyssalthreadspresentatday
s were covariates. The null hypothesis was that variations
30 in agitation rate had noeffectontherateofbyssalthread
production by D. polymorpha. Because mussel SL was
CO
(A 20 enteredintotheanalysisasacovariate,andbecauseatest
CD for homogeneity ofthis covariate showed no significant
CCO 10 differences between treatment groups, variation in SL
CD between treatments was not considered to be a con-
40 80 120 160 foundingelement in the statistical analysis.
Peg (torr)
FigureI. Theeffectofexposuretovaryingoxygentensionsonbys- Results
sogenesis by specimens ofthe zebra mussel (Dreissena polymorpha)
whenexposedtoPo2levelsof7.7, 15.4, 23.1, 30.9,and 154.3torr. (a) Responsetohypoxia
Cumulativedailymeannumberofnewbyssalthreadsproducedovera
21-dayexperimentalperiod(oruntil 100%samplemortality),(b)Mean Over the 21-day experimental period, specimens of
numberofbyssalthreads(95%confidencelimits)producedinanewly Dreissena polymorpha produced byssal threads at a
formedzebramusselbyssalcomplexfollowing7daysofexposure. slower rate when exposed to low Po2 levels of 7.7 and
15.4 torr than at higher levels of 23.1, 30.9, and 154.3
ANCOVA
aquarium was fixed on the reciprocating plate ofa New torr (Fig. la). Repeated measures indicated
RW-
Brunswick Scientific Co. waterbath shaker(model
650). A constant water temperature (25C) was main- TableI
tained in the aquaria by using the temperature control
system ofthewaterbath. Thisarrangement made it pos- RepeatedmeasuresANCOVAexaminingtheeffectofvariations in
sible to keep the submerged horizontal stage and at- partialpressureofoxygen(POi/andlime(Day.ilonby.s.salthread
productionbyDreissenapolymorphaovera "-dayexp<>.utreperiodill
tached musselstationarywhilethewater-filledaquarium 25C
was reciprocally displaced over a horizontal distance of
4cm. The fluid medium in the aquaria was maintained Effect
at a depth of 10 inches and reciprocally displaced at a
rate of CPM (cycles per minute), 10 CPM, 15 CPM,
30 CPM, or 40 CPM. Frictional forces caused by water
movement agitated the stationary mussel with a two-
phase alternating force. Exposure ofindividual mussels
416 M. CLARKE AND R. F. McMAHON
100
E 80
z
TJ
J 60
0)
TwO 40
55
>,
CD
0V) 20
10 12 14 20
10 12 14 16 18 20
Days
Days
Figure 2. Daily mortality (as percentage of .ample) ofthe zebra
mussel (Dreisscna polymorphd) when exposed to Po^ levels of 7.7, Figure 4. Cumulative daily mean number ofbyssal threads pro-
15.4. 23.1, 30.9,and 154.3ton-overa 21-u.iy experimental period, or ducedbyspecimensofthezebramussel(Dreissenapolynwrpha)overa
until 100';? samplemortalityoccurred. 21-day period, when exposed to agitation rates of0, 10, 15, 30, and
40cyclesperminute(CPM).
that Po2 significantly influenced the rate ofbyssogenesis
over the first 7 days ofexposure (Table I). An LSD test exposed to 7.7 and 15.4torrled to increasingly largedis-
indicated that the mean rate ofbyssogenesis was signifi- paritiesinsamplesizesbetweentreatmentgroupsastime
cantlygreater(P< 0.05) formusselsexposed to high Po2 progressed.
(23.1, 30.9,and 154.3torr)than forthoseexposedtolow There was very little new byssal thread formation by
(PFoig2.(7I.b)7.aTnhde1n5u.l4lthoyrpr)o,thoevseirstthheatfiorsxty7gednaycsonocfeenxtproastuirone zmeubrma msuursvsievlasletxipmoesseodft1o57a.n7dor161d5a.y4st.orHroowveevrert,hetympaixcia-l
had noeffecton the rateofbyssal thread production was byssal thread production curves, showing a steady in-
therefore rejected. As a result of differing production crease in the number of threads produced with time,
rates, specimens held at 23.1, 30.9, and 154.3 torr had were recorded at a Po2 of23.1, 30.9, and 154.3 torr(Fig.
significantlymorenewbyssalthreadsintheirbyssal mass la). For mussels exposed to 7.7 or 15.4 torr, mean sur-
after 7 days exposure than those held at 7.7 or 15.4 torr vival times were 5.2 and 5.8 days, and maximum sur-
(Fig. Ib). Mean byssal thread number is reported after vival times were 15 and 16 days, respectively. At 23.1
the first 7 days only, because high mortality in samples torr, 33.3% sample mortality was observed by the end
ofthe21-dayexperimental period. Mortalitydeclinedto
18.2% at a Po2 of30.9 torr. No mortality was observed
in the sampleofmusselsexposedat 154.3 torr(Fig. 2).
100
At 7.7 torr, 14.3% ofthesamplereleased from thebys-
sus, relocated, and byssally reattached within the experi-
mental chamber prior to death or the end ofthe experi-
mental period (whichever came first). This figure was
28.6% at a Po2 of 15.4 torr, 67.8% at 23.1 torr, 53.6% at
30.9 torr, and 73.4%. at 154.3 torr(Fig. 3).
Responsetoagitation
Byssal thread production was inhibited by increasing
agitation rates. Maximal byssal thread production over
6 8 10 12 14 16 18 20 the 21-day exposure period was achieved at an agitation
rate of CPM, and minimum thread production oc-
Days curred at 40 CPM (Fig. 4). Repeated measures AN-
Figure3. Percentage ofthe zebra mussel (Dreisscnapolymorpha) COVA indicated that agitation rate had a significant
pslaamtpe,leprdiroorpptiongdefartohmotrhethbeysseanldhoolfdftahset2a1n-ddaryeloecxapteirnigmoennttahlepplearsitoidc effect on byssal thread production rate over the 21-day
(whichevercame first), when exposed to Po? levelsof7.7, 15.4, 23.1, test period. Thisresulted in rejection ofour null hypoth-
30.9,and 154.3torr. esis. Production rate varied significantly with the re-
ZEBRA MUSSEL BYSSOGENESIS 417
TableII
RepeatedmeasuresANCO\'A examiningtheeffect<>lvariationsin
agitationrale(CPM)andlime(Oars)onhyssalthreadproductionby
specimens<>/ Dreissenapolymorphaowra21-dayexposureat25C
Effect dfEffect MSEffect
A)Agitation
418 M. CLARKE AND R F. MrMAHON
a03
ZEBRA MUSSEL BYSSOGENESIS 419
tolifein relativelystable,largebodiesoffreshwater, usu- mussel,Drei.ssenapolymorpha(PaKas). Pp501-514inProceedings
allyatdepthsbelow 3 m(Claudiand Mackie, 1993).The coofntshienFSoeuarGthraInntteIrnnstaittiuotnea.lMaY.deihsroan.MuWsIs.el Conference 1994. Wis-
tendency for agitation to suppress byssogenesis in D. Clarke, M., and R. F. McMahon. 1996a. Comparison ofbyssal at-
polymorpha suggests that this species would be unlikely tachmentindreisscnidandmytilidmussels:mechanisms,morphol-
to form functional byssal holdfasts in wave-influenced ogy, secretion, biochemistry, mechanicsand environmental influ-
littoral regions. In fact, we observed, but did not quan- ences.Malaeol. Rev. 28.Inpress.
tmiufys,sealsclteoarsptoenntdaennecoyusfloyrrienlecarseeasferdomnutmhbeebrysssoufs wzehberna Clarokne,byMs.s,ala-ntdhreRa.dF.prMocduMcathioonn.inIt9h9e6bz.ebraEffmeucstsseolf(cDurreriesnstenvaelpoocliyt-y
morpha}.Can.J. Zool.74:63-69.
exposed to high levels of agitation. Thus, mussels ini- Clarke, M., and R. F. McMahon. I996c. Effect oftemperature on
tially settling in wave-influenced littoral regions may de- byssal thread production in the zebra mussel (Dreissena poly-
tach from original attachment sites and move to deeper morpha).Am. Malaeol Bull. 12.Inpress.
waters. Dispersal ofshallow-settling (<1 m)juveniles to Claudi,R.,andG. L.Mackie. 1993. PracticalManualforZebraMus-
greater depths has been reported for D. polymorpha selMonitoringandControl. LewisPublishers,BocaRaton,FL.227
(Mackie el at., 1989). M. edulis occurs in both marine (larpgpe.r,J. R.E.,and D. K. Landenberger. 1971. Theeffectofstorms
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Asanadaptation, M. edulisiscapableofgoodregulation Kaster, J. L. 1995. Use ofan air injection system to control zebra
of oxygen uptake with progressive hypoxia and has a mussels. ZebraMusselResearch TechnicalNotesZMR-2-18. U.S.
high tolerance for hypoxia (Bayne et al., 1976). In con- Army EngineerWaterways ExperimentStation. Vicksburg, MS. 4
thryapsto,xzieabcraommpuassreeldstaorethreelmataijvoerliytiyntoofloertahnetromfaarnionxeiaanodr Lee,sPtPr.Ce.ngYt.,hoSf.bSy.ssLa.lrLeiamt,taacnhdmenMt.bDy.blOuweemnuss.sel1s98(9M.yliTlhuseedrualtiesaL.n)d.
freshwater bivalve species (Matthews and McMahon, Con J. Zool.68:2005-2009.
1994) and display little or nocapacity to regulate rate of Mackie, G. L., W.N. Gibbons, B. W. Muncaster, and I.M. Gray.
oxygen uptake(AlexanderandMcMahon, unpub.data). 1989. TheZebra Mussel. Dreissena polymorpha: A Synthesisof
The poor hypoxia tolerance ofD. polymorpha prevents EuropeanExperiencesandPreviewforNorthAmerica.GreatLakes
its penetration into oxygen-depleted hypolimnetic wa- Smeecntti,onQ,uWeaetnesrPRreinstoeurr,cTeosrBornatnoc,hO,nOtnatriaor,ioCaMninaidsat.ry76ofptph.eEnviron-
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D.polymorphaandM. edulistoenvironmental variables Finoeuar)thunIdnetrerenxattiroenmaelhZyepborxaia.MuPsps.el23C1o-n2f4e9reinncePr1o9c9e4e.diWnigsscoonfsIihne
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