AMER. ZOOL., 36:339-363 (1996)
The Physiological Ecology of the Zebra Mussel, Dreissena polymorpha, in North America and Europe1
ROBERT F. MCMAHON Center for Biological Macrofouling Research, Department of Biology, Box 19498, The University of Texas at Arlington, Arlington, Texas 76019
SYNOPSIS. The zebra mussel, Dreissena polymorpha (Pallas), was intro duced into North America in 1986. Initial North American (N.A.) studies suggested that physiological responses varied between N.A. and European populations. However, literature review indicates agreement on most as pects of physiological "adaptation including: respiratory responses; hyp oxia/anoxia tolerance; salinity limits; emersion tolerance; freezing resis tance; environmental pH limits; calcium limits; starvation responses; and bioenergetic partitioning. The main differences among N.A. and European mussels appear to be elevated upper thermal limits and temperatures for optimum growth among N.A. populations. N.A. zebra mussels probably originated from the northern shore of the Black Sea in the warmest por tion of the mussel's European range. However, most European physio logical data come from northern Europe where populations may be adapt ed to colder temperatures. Alternatively, N.A. research suggests that mus sels may have a capacity for seasonal temperature acclimatization such that responses recorded in warmer N.A. waters may be different from those recorded in northern Europe even after short-term laboratory accli mation. Studies of genetic variation and physiological response among European and N.A. D. polymorpha populations are required to elucidate the basis for physiological differentiation. Recently evolved D. polymor pha has poor resistance adaptations compared to unionacean and sphaeriid bivalves with longer freshwater fossil histories. Poor resistance adapta tions make it less suited for stable habitats, instead, its high fecundities, early maturity, and rapid growth are adaptations to unstable habitats where extensive resistance adaptations are of little value.
INTRODUCTION remarkable. It is now in all of the Great The European, freshwater, zebra mussel, Lakes> * e Fin£eT Lakes- Oneida Lake and Dreissena polymorpha (Pallas, 1771) was Lake Champlain, the St. Lawrence, Hud introduced into the Lake St. Clair-Detroit son> Seneca, Mohawk, Susquehanna, Ilh- River region of the Lawrentian Great Lakes nois' Mississippi, Ohio, Tennessee, Cum- of North America (N.A.) in 1986 (Hebert berland, Arkansas, Atchafalaya, Allegheny, etal, 1989; Mackie et al, 1989). The likely St. Croix> Kanawha, White and Neosha source population was the lower Dnieper or Rivers and New York' s Erie Barg e Canal Bug River, both opening on the northern (Zebra Mussel Information Clearing House, shore of the Black Sea near the Ukrainian 1995; United States National Biological port cities of Kherson and Nikolayev (Spi- Service, 1995). It has also invaded smaller, die et al., 1994; McMahon etal., 1994). Its isolated inland rivers and lakes, 54 popu dispersal through N.A. freshwaters has been lations recorded from isolated lakes in six states bordering the Great Lakes (United States National Biological Service, 1995). • From the Symposium Biology Ecology and Phys- ^ zehm mussej hag colonized N A wlogy of Zebra Mussels presented at the Annual Meet ing of the American Society of Zoologists, 4-8 Janu- aquatic environments of widely varying ary 1995, at St. Louis, Missouri. physico-chemical characteristics, suggest 339 340 ROBERT F. MCMAHON ing capacity for physiological compensa erature on the physiological adaptation of tion and/or toleration. Preliminary estimates D. polymorpha on both continents. Topic of its resistance and capacity adaptations areas include: temperature responses; respi suggest that it will eventually colonize the ratory responses; hypoxia/anoxia tolerance; majority of permanent inland freshwater in salinity tolerance; emersion and freezing re the U.S. and southern Canada (Strayer, sistances; pH and Ca2+ concentration limits; 1991; Electric Power Research Institute, starvation resistance; and bioenergetic par 1992; McMahon, 1992; Claudi and Mackie, titioning. 1993). Because it is both an ecological (Hebert TEMPERATURE RESPONSES et al, 1991; Maclsaac et al, 1991, 1992; Temperature responses among European Mackie, 1991; Nalepa et al, 1991; Haag et and N.A. zebra mussels initially appear in al, 1993; Gillis and Mackie, 1994; Schloes congruent. However, analysis of published ser et al., 1996) and macrofouling threat results suggests general similarity with a (McMahon, 1990; McMahon and Tsou, few notable exceptions. In Europe, spawn 1990; Electric Power Research Institute, ing temperatures, usually recorded as tem 1992; Miller et al., 1992; Claudi and Mack perature of first appearance of eggs or lar ie, 1993), N.A. biologists, environmental val stages in the plankton, range from 10°C ists, government officials, and industrial to 17°C (Sprung, 1992). In German lakes, and agricultural managers are assessing oocyte number and ovary volume decreased their waters' susceptibility to zebra mussel markedly after initiation of spawning at colonization. Development of accurate col 12°C (Borcherding, 1991). A spawning onization risk analyses requires a thorough threshold of 12°C has also been recorded in understanding of the mussel's physiological the Rhine River, Germany (Neumann et al, resistance and capacity adaptations as will 1992). In contrast, initial spawning temper future studies of its ultimate impact on N.A. atures in N.A. have been greater than 12°C. freshwater and development of nonchemi Weekly to biweekly examination of male cal mitigation/control strategies for its ma and female gonad sections in mussels from crofouling (Electric Power Research Insti western Lake Erie indicated that spawning tute, 1992; Miller et al, 1992; Claudi and first occurred at 22-23°C even though ve Mackie, 1993). liger larvae were first observed at 18°C. Ve Early studies indicated that the resistance liger abundance declined sharply in the fall and capacity adaptations of N.A. zebra at water temperatures below 18°C (Garton mussels were divergent with those of north and Hagg, 1992). Veligers were first re ern Europe, particularly thermal responses corded at 22°C near the southern shore of (Iwanyzki and McCauley, 1992; McMahon western Lake Erie (Nichols, 1996) and at et al, 1994; Nichols, 1996). If differences 18°C in western and central Lake Erie, ve exist, they may result from the majority of liger density again declining rapidly after European studies being carried out on mus water temperatures fell below 18°C (Fral sels from waters which are colder (for a re eigh et al, 1992). A similar 18°C threshold view of European research see Mackie et for first veliger appearance occurred al, 1989) than those colonized by mussels throughout eastern Lake Erie in 1990 (Ries in N.A. Their suspected origin from just sen et al, 1992). In contrast, on the south ern shore of the Lake Ontario, veligers were north of the Ukrainian Black Sea in the 3 warmest portion of D. polymorpha's Euro present in 1993 in low densities (<300 m~ ) at water temperatures as low as 3.4°C, and pean range (Spidle et al, 1994; Marsden et 3 al, 1996), suggests that N.A. mussels may increased markedly (>3,000 m~ ) only after be adapted to warmer environments. 18°C was reached (R. E Green, personal communication). These data suggest that In order to provide a foundation for fur spawning in D. polymorpha may start at ther investigation of physiological adapta 12°C, but is maximized above 17-18°C. tion in D. polymorpha, and assess possible Similarly, in a Polish lake, veligers oc differences between N.A. and European curred in minimal densities at temperatures populations, I have reviewed available lit PHYSIOLOGICAL ECOLOGY OF ZEBRA MUSSELS 341 as low as 8°-10°C, but reached peak levels development at higher temperatures is as only above 20°C (Kornobis, 1977). Thus, it sociated with increased larval growth rates appears that limited spawning many occur (Sprung, 1989). Temperature effects on lar below 17-18°C in both N.A. and European val development have not been investigated populations. When minimal veliger densi in N.A. ties prevent effective sampling at low tem Zebra mussel growth rates are tempera peratures, it may appear that spawning is ture dependent. The threshold for initiation initiated above the 17-18°C threshold of adult shell growth in English and Rus where spawning activity is maximized. sian reservoirs was 11°-12°C (Morton, Thus, initial spawning temperatures of 17 1969). In European mussels, ingestion rates 21°C are also reported among a number of are maximized at this temperature (Walz, European populations (Sprung, 1992). 1978a). Temperature for maximum adult Spawning temperatures therefore appear to growth also falls within the 10°-15°C range be similar in Europe and N.A., being initi optimal for tissue growth (Walz, 19784>) ated at ~12°C and maximized above 17 and 10°-22°C range for maximal filtration 18°C. The 17°-18°C peak spawning thresh rate (Reeders and Bij de Vaate, 1990). old corresponds to the optimum tempera Temperature effects on shell or tissue ture (18°C) for larval development (Sprung, growth rate have not been investigated in 1987) and peak pediveliger settlement N.A. zebra mussels. However, population (18°C) (Piesik, 1983; Afanas'yev and Pro age/size structures indicate that shell tasov, 1988). growth rates were >1 cm/yr in Lake Erie Occurrence of veliger larvae in Lake On (Griffiths et al., 1991) where temperatures tario at 3.5-11°C (R. F. Green, personal remain for long periods above the 10°-15°C communication), below the 12°C threshold range considered optimal for shell growth for gamete maturation and spawning among in Europe (Walz, 1978&). Surface water both European (Borcherding, 1991) and temperatures fell within 10°— 15°C an aver N.A. zebra mussel population (Garton and age of only 50 days per year (range = 34— Haag, 1992), suggests that they were not 61 days) over 1992-1994 in Lake Erie at the result of a winter spawning event, par Buffalo, NY, yet mussels maintained high ticularly as fertilization is impossible below rates of summer growth in this area (G. L. 10°C (Sprung, 1987). Instead, declining fall Dye, personal communication). They also water temperatures may have arrested ve maintained rapid shell growth rates in the liger development, causing them to remain lower Mississippi River at Baton Rouge, in the plankton during winter months. Win LA (T. H. Dietz, personal communication), ter arrest of veliger settlement and meta in waters which fall below 15°C for only a morphosis has been reported in both Europe few winter months (Hernandez et al., (Kirpichenko, 1964; Lewandowski, 1982) 1995). Further studies of temperature ef and N.A. (Nichols, 1996) and probably ac fects on N.A. zebra mussel shell and tissue counts for appearance of veligers during pe growth are clearly required. riods when spawning and fertilization are European and N.A. estimates of zebra impossible (<12°C) in both N.A. (R. F. mussel thermal tolerance limits also dis Green, personal communication) and Eu agree. Northern European data indicate an rope (Sprung, 1992). incipient upper lethal limit of 27°-28°C Temperature influences larval develop based primarily on field studies (Afana ment and adult growth rates. European data s'yev and Protasov, 1987; Testard, 1990; suggest that 10°-26°C is required for suc Jenner and Janssen-Mommen, 1992). In cessful fertilization (Sprung, 1987) and contrast, N.A. Great Lakes mussels could 12°-24°C, for larval development with be held indefinitely in the laboratory at 17.3°C being optimal (Sprung, 1987). De 30°C, 31°C being the incipient upper lethal velopment time declines with increased limit (Iwanyzki and McCauley, 1992; Mc temperature; metamorphosis to the D-sha Mahon et al. 1994) (Fig. 1A). Observations ped veliger requiring 90 hr at 12°C, but in the lower Mississippi River suggest that only 31 hr at 24°C (Sprung, 1987). Rapid mussel populations thrive where tempera model creas crease Thus pat bee ma independen temperatur et othe Protasov al., 34 derive temperatur a temperatur (vertica I o etal, limi mussel ture FIG n t f differen al., Survivorshi acclimatio Survivorship 2 A . =
l ( e 1 1995) n toleranc s t 33.98 Europea r regressio 1994) develope equivalen reac presente d . , Europea e 250 150 200 100 Chroni toleranc - - fro l 1988) d exponentiall 0.0517(S 0.944(l axis 50 s acclimatio 0 fo t e e rate , m 1987 o acclimatio 3 h a , ) V\\\\v^^^ 1 e r 2 condition \ I durin o f \ t \ ChronicTemperatureToleranc Treatmen lon (ET 3 d 50 multipl variable + s . c i e n Acclimation , (horizonta — ^ n Temperature an r indicatin n o n population excee n d p 0.0579(A temperatur t % n th studie e t ; equatio (McMaho 2 (h d g g E time Testard f sampl ) 3 o acut chroni L e period N.A an tex n N.A e i ) T (labele linea n y n i temperatur 3 wit d e t d s mm) t s (afte l uppe n s 3 o Temperatur e shel 30° axis whic s c repor . mortalit . °C increas g zebr mussel (long-term r n n regressio , a 10 s T d h 1990) modelin th r 4 s a o McMaho ) r ) increase n i e (Afanas'ye C 3 an therma . n l c (AT) et n lengt t n uppe (Hernande h e respons 30° t a °C d holdin chronic woul mussel y afte al., 5 s (vertica 3 (McMaho n e . ) e ) C l However mode wit , limit exposur r h an exposur ROBER n r 1994) prio (Tourar g e therma et (SL e 6 d effect d (°C curves) g 3 expo al., extir zebr d s h l v ther l s r axis presente o de temperatur ha in an z ) ) f 1994) 7 T e a et : th t F n d a e . s s s - , - - - - o i l , Respons e LT . constan zebr MCMAHO . B d 5 0.0167° ele tur Europea greate opposite threshol t (Fig tha (Afanas'ye ar slop mens 30 les wer ship sur 1993) 10—5 1992 i 0 o a . a e o o "s n Effect e constan mussel 0 Acut acclimatio e s th d n s les 3 e 37 estimate o h e fo e fo t e . s 1. temperature letha 1) curve nearl ) e predicte fo , 0 . whil respectivel tex f r r Value 34 41 3 35 36 40 h 39 s acclimatio tha 5 s i r r e o C . r 8 N.A d toleran 50 0.0 N n h tha uppe , S r n t Dreissena o t l f mussel (afte dependin s temperature acut 0° r n derive Temperatur v o y L t d 0 n e (Jenne f warmin reporte % an 0.2° t fro Tolerance Acute instantaneousl (a 31°C . _ N.A indicate 0.2 reporte s . C r e adul d r sampl o McMaho s exposur letha b m t d labele d t f Protasov th C tha fro Temperature o LT y 0 y s polymorpha. . n 30° min" thi mussel tolerate 0.4 (Fig , . r t the Temperature e d state an zebr m s g l metho d d (horizonta — fo g limit s n 5 e a o e o fo tha 0 s rate n smalle t mortality e (estimate d mode C multipl n et y o r 0 . Increas n Janssen-Mommen respons 1 r Europea 1A) temperature range acclimate a 0.6 (McMaho acclimatio Europea . al., t , mussel d I Acclimation s large s 1987) o hav d s tolerate y n rangin 33° A letha 1993) f contrast e l Temperatur . probits) l 0 ar Th linea r axis . e Hour individuals 0.8 d e curves r e fro bee d e ) specimen C . n e (°C/mi wer Survivor generall s tempera . n ) s s r negativ mussels fo l expose afte increasin regressio ^36° mussel d regard s n d 0 g survive m speci n . n et Curve i 1.0 fro ) mod r stat , o r 50 e a les prio t n af fo al, e th n
t a m C 0 y d n e g d e s s e s r - - s - r . , , PHYSIOLOGICAL ECOLOGY OF ZEBRA MUSSELS 343 fected by temperature increase rate (TIR) at time of collection (Fig. 2, Hernandez et and prior acclimation temperature (AT) as al., 1995), indicative of longer-term, sea follows: sonal "acclimatization" of thermal toler ance (acclimatization is defined as a longer- In LT50 in °C term, reversible, phenotypic adjustment of = 3.603 + 0.026(ln TIR in °C/min) physiological response to an environmental + 0.0036(AT in °C). variable that is not readily influenced by LT50 increases exponentially with increas shorter-term laboratory acclimation to that ing warming rate and linearly with increas variable). Thus, mussels seasonally accli ing acclimation temperature (Fig. 1). matized to cooler ambient conditions have Slower warming rates induce mortality at lower thermal tolerances than those season lower temperatures, warming rates of ally acclimatized to warmer ambient con 0.05°C min-'-0.0333°C min"1 inducing ditions even after standard laboratory tem 50% sample kills at temperatures of 33.5 perature acclimation (Fig. 2). There is cir 38°C depending on acclimation state (Fig. cumstantial evidence for seasonal acclima IB). tization in European mussels. In the Volga The basis for elevated thermal tolerance River where downstream veliger dispersal among N.A. zebra mussels has been debat precludes genetic race formation, mussels ed. Differences may be due to different Eu from warmer, southern river reaches were ropean and N.A. experimental protocols. more thermally tolerant than those from Alternatively, they could be genetic and/or cooler, northern reaches (Smirnova et al., ecophenotypic. Because N.A. zebra mussels 1992). Temperature acclimatization could are likely to have originated from the partially account for thermal tolerance vari warmest portion of the species' European ation among European and N.A. popula range (Marsden et ah, 1996), they could tions, particularly as northern European have a genetically elevated thermal toler specimens were likely to have been drawn ance (McMahon et al., 1994) relative to from seasonally cooler waters than N.A. Northern European populations. Capacity mussels (Iwanyzki and McCauley, 1992; for rapid temperature adaptation has been McMahon et al., 1994). Recent evidence demonstrated for a zebra mussel population that the upper thermal limits of European in a thermal discharge, which, within 8-10 mussels (Tourari et al., 1988) and N.A. years, developed allele frequencies at four mussels are similar at 30°C (McMahon, et of seven loci significantly different from al., 1994) suggests that seasonal acclimati those of a thermally unaffected source pop zation may account for the majority of vari ulation (Fetisov et al., 1991). Similarly, ze ation among N.A. and European studies of bra mussels from the much warmer lower thermal tolerance. Mississippi River (30-31°C during summer Temperature also affects zebra mussel months) tolerated 33°C longer than did hemolymph osmolarity, ion concentrations more northern Niagara River mussels, sug and ion flux. At 4-5°C for 51 days, mussels gesting that they were a thermally tolerant decreased hemolymph Na+, Cl~ and os physiological race (Hernandez et al., 1995). motic concentrations and increased Ca2~ The apparent capacity of D. polymorpha for concentration compared to those held at thermal selection supports the contention 20°-25°C (Scheide and Boniaminio, 1994). that N.A. mussels may be genetically more Hemolymph ion concentrations in individ thermally tolerant than northern European uals acclimated to 20°-25°C changed less mussels. relative to fresh caught individuals than The thermal tolerance of zebra mussels they did in cold-acclimated individuals. drawn from the lower Mississippi River Similar responses occurred in cold-accli also had a seasonal component resistant to mated unionids (Scheide and Boniaminio, laboratory temperature acclimation. After 1994). Transferral of 20°-25°C acclimated mussels to 4°-5° initially resulted in a net laboratory acclimation to 5°, 15° or 25°C, + their thermal tolerance remained positively efflux of Na and Cl", perhaps due to met correlated with ambient water temperature abolic reduction in capacity for active up 344 ROBERT F. MCMAHON
70 o o 5°C Acclimated A A 15°C Acclimated I 60 • D 25°C Acclimated O D o 1 CO 50 • CO +-* [ • • !c 30 t D [ 00 ..J • D O o o 20 ' P > _ » • • ' 10 '6 4 > n 10 15 20 25 30 Water Temperature at Collection (°C) FIG. 2. Effects of water temperature at time of collection (horizontal axis) and laboratory acclimation temper ature (5°C acclimated = open circles, 15°C = solid triangles, 25°C = open squares) on mean hours survived (vertical axis) on exposure of zebra mussels (Dreissena polymorpha) to a lethal temperature of 33°C. Vertical bars about means are standard errors. Lines represent best fits of least squares linear regressions relating mean survival times to ambient water temperature at collection (5°C acclimated = short dashes, 15°C = solid line and 25°C = long dashes). Intercepts and slopes of regressions for 5°C and 15°C acclimated individuals are not significantly different (P < 0.05), while the regression slope for 25°C acclimated mussels is greater (P > 0.05) than that of 5° and 15°C acclimated individuals (after Hernandez et al., 1995). take. However, after 51 days, net Na+ and through October (Lyashenko and Karchen Cl" losses approached zero, suggesting that ko, 1969). An average "b" of 0.63 was new, lower equilibrium Na+, Cl" and os computed for zebra mussel based on com motic concentrations had been reached bined data of several European authors (Al (Scheide and Boniaminio, 1994). Zebra imov, 1975). A value of 0.82 can be com mussel osmotic and ionic regulation is re puted from the data of Quigley et al. (1992) viewed in this volume by Dietz et al. for N.A. mussels. Zebra mussel "b" values (1996). fall among those of other freshwater mol luscs. Alimov (1975) recorded an average RESPIRATION AND METABOLISM "b" of 0.721 (±0.026) for freshwater bi Zebra mussel O2 consumption rates are valves in the former U.S.S.R. Hornbach essentially similar to those of freshwater (1985) reported "b" to range from 0-1.24 unionid and sphaeriid bivalves (Alimov, among 28 sphaeriid species while "b" val 1975), suggesting these groups have similar ues ranging from 0.25 to 1.45 occur among metabolic maintenance demands. Oxygen a wide variety of freshwater bivalves (Bur consumption rates (Vo2) are related to in ky, 1983). dividual dry tissue mass (M) as follows: Respiratory responses to acute tempera b ture change and prior temperature accli Vo2 = aM , mation have been recorded in N.A. and Eu where "a" and the exponent, "b", are con ropean zebra mussels. Mussels from the stants relating dry tissue mass to Vo2. Val western basin of Lake Erie displayed partial ues of "b" in this equation model increase respiratory temperature compensation such in Vo2 with unit increase in tissue mass. that Vo2 recorded over 5°-3O°C was signif They ranged from 0.66-0.84 in European icantly decreased in 25°C relative to 5°C zebra, mussel populations from February and 15°C acclimated individuals (Fig. 3, Al PHYSIOLOGICAL ECOLOGY OF ZEBRA MUSSELS 345 3.5 O 5°C Acclimated 3.0 A I5°C Acclimated D 25°C Acclimated 2.5 E 2.0 1.5 1.0 0.5 10 15 20 25 30 35 40 45 TEMPERATURE in °C FIG. 3. The effect of exposure temperature (horizontal axis) and prior acclimation temperature (5°C = circles, 15°C = triangles, 25°C = squares) on the oxygen consumption rate of standard sized individual of zebra mussel, 1 1 Dreissena polymorpha, in microliters of oxygen per mg dry tissue weight per hour (u.1 O2 mg" h" ) (vertical axis) (J. E. Alexander, Jr. and R. F. McMahon, unpublished data). exander and McMahon, unpublished data). climation is required in zebra mussels in or Among 5°C acclimated specimens, maxi der to resolve such contradictory data. mal Vo2 occurred at 30°C, between 30° and Qlo values relating increase in Vo2 to 35°C in 15°C acclimated individuals, and at temperature (Q,o is a computed value indi 35°C in 25°C acclimated individuals (Fig. cating the factor by which Vo2 increases 3). Temperatures of maximum Vo2 (Fig. 3) with a 10°C increase in temperature. It can and acute upper lethal temperatures on ex be calculated over any temperature range) posure to slow warming (i.e., 0.0167°C/60 have been reported for zebra mussels in Eu min, Fig. IB) correspond, suggesting that rope and N.A. (Table 1). Both European declines in Vo2 at higher temperatures (Fig. and N.A. Q10 data indicate that Vo2 increas 3) are due to acute thermal stress. es more rapidly with increasing temperature European and N.A. data on zebra mussel in the lower portion of the mussel's ambient respiratory responses to acute temperature range (5°-20°C) than at higher temperatures variation are similar. Vo2 in freshly field (20°C-30°C) (Alimov, 1975; Dorgelo and collected European mussels was maximized Smeenk, 1988; Quigley et al., 1992; Alex at 25°-35°C (Mikheev, 1964; Lyashenko ander and McMahon, unpublished data) and Karchenko, 1989). Respiratory re (Table 1). From 5° to 20°C, Q10 values are sponse to temperature was similar at differ generally greater than 2.0 (Table 2), sug ent times of the year (Mikheev, 1964; gesting active metabolic augmentation. Ac Lyashenko and Karchenko, 1989), suggest tive increase in metabolic rate up to 20°C ing little capacity for metabolic temperature may be responsible for the marked increase compensation, a result contradicting obser in mussel metabolic demand during increas vations in N.A. mussels (Fig. 3). Alexander ing spring water temperature in Europe et al. (1994) also found little evidence of (Lyashenko and Karchenko, 1989) and respiratory compensation in Lake Erie ze N.A. (Quigley et al., 1992). bra mussels acclimated to 10°, 18° or 26°C. Seasonal studies of respiration rate have Further study of respiratory temperature ac been carried out among European and N.A. 346 ROBERT F. MCMAHON TABLE 1. Ql0 values estimating the relative increase sus nonprotein catabolism in zebra mussels. in oxygen consumption rate over a 10°C ambient tem During early spring and fall at temperatures perature increase computed over different temperature ranges and for different levels of temperature accli below 16°C, molar ratios of O2 consumed mation in the zebra mussel, D. polymorpha. to nitrogen excreted (O:N ratio) in Lake St. Clair mussels ranged between 29.7 and 48.3 Respiratory Q,o value (Quigley et al, 1992), indicative of 20% Alexander and McMahon, unpublished data 39% of metabolic demands being supported Other Temperature 5°C 15°C 25°C observa by nonprotein catabolism {i.e., carbohydrate range Ace. Ace. Ace tions"^1 and lipid catabolism, computation based on 5°-10°C 4.79 1.53 0.81 3.24a Bayne, 1973). During May through August 10°-15°C 1.81 4.80 4.15 3.47" at temperatures above 18°C when spawning 15°-20°C 2.45 1.67 3.03 2.23" was likely to be maximized, O:N ratios fell 20°-25°C 2.03 2.28 2.29 1.59a 25°-30°C 1.63 2.29 1.37 1.46a to 16.0-22.2, indicative of increased depen 30°-35°C 0.21 0.85 1.84 dence on protein catabolism (Quigley et al, 35°-40°C 0.15 0.10 0.05 — 1992) (7%-13% of catabolism dependent 10°-26°C — 1.96b on nonprotein metabolites, computation 7.5°-19°C — — — 2.3= d based on Bayne, 1973). Mid-summer de 10°-20°C — — — 3.5 creases in tissue mass and nonprotein ca aAlimov, 1975. tabolism also occur in European zebra mus b Quigley et ai, 1992. sels. During winter, low food availability 'Dorgelo and Smeenk, 1988. "Alexander et al., 1994. may prevent mussel catabolism from being completely supported by assimilation, lead ing to increasing dependence on nonpro tein, carbohydrate energy stores (Walz, zebra mussels. The Vo2 of European mus sels from the Dnieper-Donbass Canal, 1979), thus accounting for the high O:N ra Ukraine, reached maximal levels during tios of 30-48 recorded in Lake Erie below peak temperature periods (Lyashenko and 8°C (Quigley et al, 1992). Karchenko, 1989), a response similar to As in a naturally spawning zebra mussel that of N.A. mussels from Lake St. Clair population from Lake St. Clair (Quigley et (Quigley et al, 1992). Interestingly, at both al, 1992), artificially spawned European sites, peak Vo2 occurred after spring water mussels had lower O:N ratios than non- temperatures rose rapidly from 7°-10°C to spawning individuals (Sprung, 1991), sug 19°-20°C, suggesting that metabolic de gesting that post-spawning individuals in mand was being partially driven by onset creased dependence on protein catabolism of maximal spawning activity above 17° for maintenance energy. During starvation, 18°C (see section on "Temperature Re freshwater bivalves deplete carbohydrate sponses"). and lipid stores, marked by a decrease in O: Turbidity also affects zebra mussel Vo2. N ratio with increasing dependence on pro Acute exposures to 0, 5, 20 and 80 NTU tein catabolism (Burky, 1983). Thus, reduc (nephelometric turbidity units) induced a tion in O:N ratios of Lake St. Clair mussels progressive decline in Vo2. Thereafter, Vo2 above the 18°C peak spawning threshold stabilized over 80 to 160 NTU at 40-70% (Quigley et al, 1992) may have been due of the rate at 0 NTU (Alexander et al., to massive allocation of nonprotein energy 1994). Zebra mussels thrive in the lower stores to gametogenesis. Reductions in tis Ohio River (Zebra Mussel Information sue ash free dry weight, and lipid content Clearinghouse, 1995) where turbidities can during July through September among Lake exceed 145 NTU (Alexander et al, 1994), St. Clair zebra mussels (Nalepa et al, 1993) suggesting that turbidity induced suppres are evidence of post-spawning reduction in sion of Vo2 is transitory with mussels ca nonprotein energy stores. During this peri pable of compensating Vo2 to ambient tur od, tissue organic carbon to nitrogen ratios bidities over naturally occurring exposure (C:N) fell from 6-7 to approximately 3.5 periods (Alexander et al, 1994). 4 (Nalepa et al, 1993). As average protein C:N is 3.25, post-spawning mussels had re Temperature may also affect protein ver PHYSIOLOGICAL ECOLOGY OF ZEBRA MUSSELS 347 duced carbohydrate and lipid energy re 1100 serves. Resulting increased dependence on 1000 | 5°C ACCLIMATED protein catabolism would yield the low O: 900 |L. [ j 15°C ACCLIMATED I N ratios recorded during post-spawning pe £ 800 i ' 25°C ACCLIMATED riods (Quigley et al, 1992). Metabolic and shell growth rates are pos j§ 500 l itively correlated with degree of individual 400 T multiple locus heterozygosity in marine bi valves (for a review see Garton and Haag, 300 1991). When tested against seven polymor 200 phic enzyme loci, the shell length of west 100 > 84 ern Lake Erie zebra mussels was positively Days correlated with increasing multiple locus 0 i I heterozygosity, but not with Vo2. Increased 5°C 15°C 25°C 5°C 15°C 25°C growth rate in highly heterozygous individ Test Temperature i Dreissena , , Corbicula , uals may be a manifestation of their in polymorpha flum/noa creased energetic efficiency (Garton and FIG. 4. Effects of test temperature (horizontal axis) Haag, 1991). However, lack of correlation and prior acclimation temperature (5°C acclimated = between metabolic rate and degree of het solid histograms, 15°C = finely cross-hatched histo erozygosity suggested that increased tissue grams, 25°C = coarsely cross-hatched histograms) on growth rates were due to increased assimi mean survivorship in hours (vertical axis) of speci lation rates in highly heterozygous individ mens of Dreissena polymorpha and Corbicula flumi nea exposed to extreme hypoxia (Po2 < 3 torr). Mean uals rather than to reduction in maintenance hypoxia survival times on the left side of the horizon metabolism (Garton and Haag, 1991). tal axis are for specimens of D. polymorpha and on the right-hand side, for C. fluminea. Vertical bars RESPONSES TO HYPOXIA/ANOXIA above histograms are standard errors of the means. There were no significant differences among mean sur European and N.A. studies indicate that vival times of different acclimation groups of C. flu zebra mussels are relatively intolerant of minea at a test temperature of 25°C, therefore, only 15°C and 5°C acclimated specimens were exposed to hypoxia or anoxia. Held in sealed chambers test temperatures of 15° and 5°C, respectively. Extreme depleted of O2 by mussel respiration, Eu hypoxia at 5°C produced no mortality among speci ropean zebra mussels experienced 100% mens of C.flumineadurin g 84 days of exposure (after mortality within 144 hr at 17°-18°C, 96 hr Matthews and McMahon, 1994). at 20°-21°C and 72 hr at 23°-24°C (Mikh eev, 1964). When anoxic for 37 hr at 22°C, mortality was greatest (100%) among acclimated individuals (Fig. 3). Congruent smaller mussels (shell length = 1-4.9 mm), with Russian results (Mikheev, 1964), larg survivorship increasing in larger size class er individuals were more anoxia tolerant es (0% mortality at a shell length = 20 than smaller individuals (Matthews and 24.9 mm) (Mikheev, 1964). Similarly, mean McMahon, 1994 and unpublished data). survival times of N.A. Niagara River mus Asian clams, Corbicula fluminea (Miiller), sels held in media depleted of O2 by N2 among the most anoxia intolerant of all bubbling ranged from 907-1005 hr 228 freshwater bivalves (McMahon, 1983a), are 428 hr and 53-83 hr at 5°, 15°C and 25°C, approximately twice as anoxia tolerant as respectively (Fig. 4). These values were zebra mussels (Fig. 4, Matthews and Mc somewhat greater than reported by Mikheev Mahon, 1994), making zebra mussels (1964). More rapid mortality in Mikheev's among the least anoxia/hypoxia tolerant of (1964) study may have been due to effects all freshwater bivalves. In contrast, fresh of toxic anaerobic end-products accumulat water unionacean and sphaeriid bivalves are ed in sealed test chambers. At test temper relatively anoxia/hypoxia tolerant (McMa atures of 15° and 25°C, zebra mussel anoxia hon, 1991). The chronic, lower lethal Po2 tolerance increased with increasing accli for N.A. adult zebra mussels is approxi mation temperature (Fig. 4), perhaps due to mately 32-40 Torr at 25°C (Johnson and a reduction in metabolic rate among warm McMahon, unpublished data), a value sim 348 ROBERT F. MCMAHON ilar to the minimum of 32 Torr required for al., 1989). In contrast, the second dreissenid larval development at 18°-20°C (Sprung, species introduced into North America, 1987). Recently transformed juvenile Dreissena bugensis Andrusov (quagga unionids are also anoxia intolerant (Dimock mussel), occurs in hypolimnetic waters and and Wright, 1993). inhabits soft substrata from which D. poly Most freshwater unionacean and sphae morpha is generally excluded (McDermott, riid bivalves highly regulate O2 consump 1993). Their profundal habitat suggests that tion, maintaining Vo2 at or near air O2 sat quagga mussels are more hypoxia tolerant uration levels even at very low Po2 (Mc and better O2 regulators than zebra mussels, Mahon, 1991). In contrast, D. polymorpha, hypotheses supported by preliminary ex like C. fluminea (McMahon, 1979), is a perimentation (Birger et al., 1978). How poor to nonregulator of Vo2. Lake St. Clair ever, further research is required to confirm mussels displayed no regulatory capacity this speculation. (Quigley et al, 1992). We have shown that both test temperature and prior temperature SALINITY TOLERANCE acclimation significantly affect regulatory European information on zebra mussel ability in D. polymorpha (Fig. 5). Degree salinity tolerance is primarily based on field of O2 regulation can be estimated by fitting observations and is somewhat divergent standardized Vo2 values {i.e., Vo2 expressed (for a review see Strayer and Smith, 1992). as a fraction of that at air O2 saturation) as In the tidal reaches of the Rhine River, the dependent variable to a quadratic equa Netherlands, maximal salinities for mussel tion against Po2 in Torr. The quadratic co occurrence were 0.6%o (Wolff, 1969). That efficient or "b2 " value of this equation es for completion of the entire life cycle was timates degree of O2 regulation, becoming 0.75%o to 1.29%o (2.1-3.7% of sea water at increasingly negative as regulatory ability 35%o) (Smit et al., 1992). Such data suggest increases (Mangum and Van Winkle, 1973). that 0.5-2.0%o is this species' chronic, up Based on "b2 " analysis, zebra mussels were per salinity limit, which corresponds to the good to nonregulators of oxygen consump salinity limits for mussel occurrence in tion dependent on test and prior acclimation northern Europe and the Black Sea region temperatures, regulation increasing with de (Strayer and Smith, 1992 and references creasing acclimation temperature and in therein). In contrast, zebra mussels occur in creasing test temperature. Thus, among 5°C, North-Baltic Sea estuaries at salinities up to 15°, and 25°C acclimated mussels, those ac 3.8%&-6.2%o and, in the Caspian and Aral climated to 5°C and tested at 25°C dis Seas, up to 6-10.2%o (Strayer and Smith, played the best (but still mediocre) capacity 1992 and references therein). Higher mus for oxygen regulation, while those accli sel salinity tolerances in the Caspian, Aral mated to 25° had essentially no regulatory and North Baltic Seas may be due to their ability at 5°C (Fig. 5, Alexander and Mc reduced tidal fluctuations. In more tidally Mahon, unpublished results). Increased O2 influenced Dutch estuaries, mussel popula regulation when cold-acclimated (Fig. 5) tions are subjected to extended tidal emer may allow overwintering mussels to sur sion. As D. polymorpha is intolerant of vive hypoxia resulting from surface ice for emersion (McMahon et al., 1993), mussels mation in lentic habitats as occurs in some may be restricted to low salinity, upper por freshwater unionids and pulmonate gastro tions of Dutch estuaries where tidal fluctu pods (McMahon, 1991, 19836). ations are dampened, leading to an under estimate of their salinity tolerance (Strayer Poor anoxia/hypoxia tolerance (Fig. 4) and Smith, 1992). A human mediated in and O2 regulatory ability (Fig. 5) may re crease in Aral Sea salinity to 14%o extir strict zebra mussels to well oxygenated pated its zebra mussel population in 1976 habitats (Stariczykowska, 1977), account 77 (Aladin and Potts, 1992). Thus, 14%c for their poor colonization success in eu may be the mussel's incipient upper salinity trophic lakes (Stariczykowska, 1984), and limit. Recent laboratory studies suggest that prevent populations from extending into N.A. juvenile and adult zebra mussels do hypoxic, hypolimnetic waters (Mackie et unpublished data). test temperatureof15°C,andCa25° C (J.EAlexander,JrandRFMcMahon th ned toleran g no the respiratoryresponstoprogressiv acclimated individuals,ansquaresfor25°C . Thedashedlinineachfigurerepresents torr) ontheverticalaxis.SolidcirclesarmeaVo greater thedegreofVo FIG. proportional toPo which Vo Po a e 2 mussel t Eve isindicatedaTorronthehorizontalaxiversumeastandardizeoxygeconsumptio zebr tolerat 5.Respirator y et n t wit ai, (Kilgou a 2 atanyonePo musse e s 1995) salinitie (D. h a (M salinit JDARDIZED 2 y responseofDreissenapolymorphatprogressivhypoxia.Inallthrefigures,medium bugensis) ). Thegreaterthdivergenc l r i an 0.8 0.2 0.8 0.2 0.4 0.6 Ob 0.6 1.0 0.4 0.4 0.8 0.2 . 1.0 1.0 s stil s 2 abov d regulation.ARespiratoryresponsetohypoxiatestemperatur e of5°C,B.at ¥< y £/-'' 2 • - . A isexpressedafractionoftheratrecordetfullairO Kepple 1/ toleranc PHYSIOLOGICA l B c considere e bein 20 20 20 4%o , A I5°CAcclimated • 5°CAcclimated • 25°CAcclimate 1993 e e hypoxiaofcompletelyoxygendependentindividual(Vo g , o wit eve 40 6 40 6 40 f d 6 t h — L ; o quag n ECOLOG Ken b 10%o les - e ofarespiratoryresponscurvabovthdashedline, 60 e a ^ 2 s - - valuesfor5°Cacclimate % , d P Y cie typica freshwate 3-8% 1968) ^ * 1^ 1974 '"" 80 O2 80 O 80 Test Test Test s (Torr) F (Reman / ZEBR o ; Gaine , l ar whil o Temperature =I5°C Temperature =5°C Temperature =25°C 100 100 1214 100 1214 f e r mos A specie typica MUSSEL e y e uppe ,'•''' an an t 120 freshwate d d individuals,trianglesfor15°C d l s Greenberg o Schlieper becaus r limit S f mos 140 2 saturation(Po r s e t bivalve freshwate o uppe , , 1971 160 1977) f 8-10% n rate(Vo r limit s ; (Fuller 2 . Green directly Uppe 2 r =159 spe o ar s 2 34 o ) in e 9 f r , , 350 ROBERT F. MCMAHON 15 20 25 30 Temperature (°C) FIG. 6. Effects of temperature (horizontal axis) and relative humidity (as indicated on individual response curves) on the emersion tolerance of zebra mussels, Dreissena polymorpha, expressed as LT50 values (i.e., estimated time in hours for 50% sample mortality, vertical axis) as computed from the multiple regression model described in the text (after McMahon et al., 1993). salinity limits of truly estuarine species are adult colonization. Salinity limits appear well above 10%o (Remane and Schlieper, somewhat lower for D. bugensis, with be 1971; Green, 1968; Gainey and Greenberg, low *=*4%o required for successful life cycle 1977). completion and maintenance of adult pop When acclimated to freshwater, Lake St. ulations. Clair zebra mussels could be induced to spawn by external serotonin application in DESICCATION AND FREEZING RESISTANCE media <3.5%o at 12°-27°C, but successful European zebra mussels are relatively fertilization required <1.75%o (Fong et al, emersion intolerant, incipient mortality oc 1996). Acclimation to 1.75, 3.5 or l%o al curring after four days in air at 20°-22°C. lowed spawning to be induced up to l%o Anaerobic, hemolymph respiratory acidosis and successful fertilization up to 3.5%o during emersion was buffered by shell (Fong et al, 1996). Early zebra mussel em CaCO3 (Alyakrinskaya, 1978). Our studies bryonic development occurs in salinities indicate that emersion tolerance (computed <6%o, and, at <4%o in quagga mussels as LT50 values, i.e., time for 50% sample (Kennedy et al, 1995). Less than 8%o was mortality estimated by probit analysis) in required for development of zebra mussel Lake Erie zebra mussels decreased expo larvae to D-hinge veligers and <6%o for nentially with increasing air temperature successful pediveliger settlement. Quagga and decreasing R.H. as modeled by the fol mussels required <4%o for development of lowing multiple regression equation: D-hinge veligers and pediveliger settlement (Wright et al, 1995). Thus, early D. poly In LT50 = 5.243 - 0.074(°C) morpha developmental stages have the same or slightly lower maximum salinity (Fig. 6) (McMahon et al, 1993). Water loss limits as adults with salinities below =6%c rates in emersed mussels increased expo required for successful spawning, fertiliza nentially with increasing temperature and tion, settlement and transformation to the decreasing R.H. At 5°, 15°C and 25°C, per juvenile and below =*l-\0%c, for successful cent of total water lost at death (total water PHYSIOLOGICAL ECOLOGY OF ZEBRA MUSSELS 351 = tissue plus extracorporeal mantle cavity emersed quagga mussels expose mantle tis water) ranged between 58% and 71% in sues for aerial gas exchange less frequently <5% to 75% R.H., levels of lethal desic than zebra mussels (Ussery and McMahon, cation similar to that of other freshwater bi 1994). Reduction in aerial gas exchange at valves (Byrne and McMahon, 1994). How high R.H. by qugga mussels could lead to ever, at >95% R.H., mean percent of total their more rapid accumulation of anaerobic water lost at death was much lower at 35 end-products to lethal levels. In contrast, 40%, suggesting that death resulted from le Ricciardi et al., (1995) found that evapo thal accumulation of metabolic end-prod rative water loss rates in D. bugensis were ucts (McMahon et al., 1993). Similar levels greater than those of D. polymorpha when of N.A. zebra mussel desiccation resistance emersed at 20°C in 10%, 50% or 95% R.H. have been reported by Ricciardi et al. The quagga mussel's profundal habit (1995). (McDermott, 1993) exerts little selection Based on LT50 values, zebra mussel pressure for emersion tolerance (Ussery and emersion tolerance times above 25°C were McMahon, 1994), thus its poorer emersion less than 100 hr regardless of R.H., increas tolerance relative to epilimnetic zebra mus ing to 100-400 hr at 5°C depending on sels is not unexpected. R.H. (Fig. 6) (McMahon et al., 1993). At a lethal temperature of 35°C, zebra These levels of emersion tolerance are far mussel emersion tolerance times were less than recorded among other freshwater greatly reduced (10—40 hr depending on bivalve species, many of which tolerate R.H.) relative to nonlethal temperatures emersion for many months (for reviews see (<30°C), but increased with decreasing McMahon, 1991; Byrne and McMahon, R.H., a result opposite that recorded at non 1994). Poor desiccation tolerance may be lethal temperatures. In lethal air tempera the reason that juvenile zebra mussels set tures such as 35°C, inhibition of evapora tling at depths <1 m migrate into deeper tive cooling at high R.H. may have reduced waters (Mackie et al., 1989). However, ex capacity for evaporative cooling causing tended emersion tolerance in mussels at low tissues to more rapidly reach lethal temper temperatures and high R.H. (Fig. 6) suggest atures (McMahon et al., 1993). that mussels could be transported long dis Juvenile zebra mussels settling in shal tances on anchor chains of ocean-going low water may migrate to greater depths to vessels, trailered pleasure craft, or aquatic avoid emersion in freezing winter air macrophytes snagged on boat trailers. Ex (Mackie et al., 1989). Adult, N.A. zebra tensive mussel anchor chain colonization mussels proved highly intolerant of aerial occurred within 24 hr on a vessel anchored freezing (Clarke 1993; Clarke and McMa in Lake Ontario (R. F. Green, personal com hon, 1993). Single (separate) individuals munication), making anchor chains a pos experienced 100% mortality within 2-15 hr sible vector for this species' introduction to at -10° to -1.5°C (Fig. 7). Among clusters N.A. (McMahon et al., 1993) in addition to of 10 mussels, representing conditions in larval transport in ship ballast water (Mack dense populations, the maximal temperature ie et al., 1989). for mortality was — 3°C. Survival times of At 15°C, N.A. quagga mussels (D. bug clustered mussels were double that of single ensis) had emersion tolerances very similar mussels at all tested temperatures (—3.0° to to zebra mussels between <5%, and 33% - 10°C) (Fig. 7). Clustering increased rela R.H., but tolerance was reduced at R.H. tive tissue mass, and therefore, time re >53% (Ussery and McMahon, 1994). Sim quired for tissues of clustered individuals to ilarly, N.A. quagga mussels were found to freeze. Tissue super cooling points were be less emersion tolerant than zebra mussels high (~-0.37° to -2.03°C), suggesting at 10°C and 95% R.H. (Ricciardi et al, lack of the tissue or hemolymph antifreeze 1995). Reduced quagga mussel emersion agents characteristic of truly freeze resistant tolerance in elevated R.H. was associated organisms (Clarke, 1993). Fifty percent with reduced evaporative water loss rates sample mortality occurred when 22% of relative to zebra mussels, suggesting that body water was frozen (Clarke, 1993), sug 352 ROBERT F. MCMAHON 30 > 48 h > 48 h LTM - Separate 25 SM100 - Separate LTM - Clustered V 20 SMIOO - Clustered E t 15 I 10 5 0 -10 -7.5 -5 -3.0 -1.5 0.0 Air Temperature (°C) FIG. 7. The effect of subfreezing air temperatures (horizontal axis) on survival times in hours (vertical axis) of the zebra mussel (Dreissena polymorpha). Histograms represent survival of individuals either singly exposed (separate) or exposed in a group of 10 clustered mussels (clustered) expressed as either hours for 50% sample mortality (LT50 estimated by the method of probits) or as hours required for actual 100% subsample mortality (SM100). Single individuals at 0°C and clustered individuals at 0° and — 1.5°C survived emersion more than 48 h (after Clarke, 1993; McMahon et al 1993). gesting a lack of cryoprotectants that allow sel Ca2+ tolerances are somewhat lower tolerance of extensive tissue freezing in in than reported for European populations tertidal mytilid mussels (Williams, 1969). (Ramcharan et al., 1992) and correspond with lower limits of 10—11 mg Ca2+/liter for CALCIUM CONCENTRATION AND PH LIMITS initiation of shell growth and 25—26 mg Zebra mussels are less tolerant of low Ca2+/liter for maintenance of moderate shell calcium concentration and low pH than oth growth (Claudi and Mackie, 1993). er freshwater bivalves (McMahon, 1991). The bases for the relatively high lower Most unionaceans grow and reproduce at a pH and Ca2+ concentration limits of zebra pH of 5.6 to 8.3 and at Ca2+ concentrations mussels have received little study. Adult above 2.0 to 2.5 mg Ca2+/liter. Many sphae mussels cannot regulate hemolymph Ca2+ at riid species are adapted to acidic, low cal < 12-14 mg Ca2+/liter. Hemolymph Ca2+ cium habitats (McMahon, 1991 and refer regulatory capacity declines below pH 6.8 ences therein). Minimum pH limits are 6.5 6.9 (Vinogradov et al., 1992). Both values for adult zebra mussels and 7.4 for veligers. correspond with the lower Ca2+ concentra Those for moderate and maximal adult tion and pH thresholds for zebra mussels growth are 7.4 and >8.0, respectively (see above). In contrast, two unionids, An (Claudi and Mackie, 1993). European mus odonta cygnea (L.) and Unio pictorum (L.), sels were absent from lakes with pH <7.3 2+ were much more tolerant of low pH and and Ca concentrations <28.3 mg Ca2+ concentration, regulating hemolymph Ca2+/liter. Population density was positively 2+ 2+ 2+ Ca at 3 mg Ca /liter and 6-7 mg correlated with Ca concentration and neg Ca2+/liter, respectively, as well as regulating 3 2+ atively correlated with PO4 ~ and NO3~ hemolymph Ca in media of much lower concentrations (Ramcharan et al., 1992). In pH than could zebra mussels (Vinogradov N.A., mussels inhabit waters S15 mg et al, 1992). Apparent inability of zebra Ca2+/liter, with dense populations develop 2+ mussels to regulate hemolymph ion and ing >21 mg Ca /liter (Mellina and Ras acid/base levels in waters of even moderate mussen, 1994). North American zebra mus acidity and calcium concentration may be PHYSIOLOGICAL ECOLOGY OF ZEBRA MUSSELS 353 associated with their restriction to waters of greater pH and hardness relative to most other freshwater bivalves (McMahon, 1991). Zebra mussel veliger larvae have pH and calcium limits similar to those of adults. Successful rearing requires media S12 mg Ca2+/liter. Rearing success is positively cor related with Ca2+ concentration, production of deformed larvae being minimized above 0 SO 100 150 200 250 300 350 400 450 500 34 mg Ca2+/liter (Sprung, 1987). A pH of 7.4-9.4 is required for successful veliger Days of Starvation development, optimal rearing success and FIG. 8. Effect of prolonged starvation on dry tissue minimal larval deformation occurring at pH weight in the zebra mussel, Dreissena polymorpha. = 8.4 (Sprung, 1987). Further studies of pH Horizontal axis is days of starvation. Solid squares are the estimated dry tissue weight of a 20 mm shell length and calcium concentration effects on D. standard sized mussel starved at 5°C. Triangles repre polymorpha are required. sent these same values in mussels starved at 15°C and squares, in mussels starved at 25°C. Lines represent RESPONSES TO STARVATION best fits of Least Squares Linear Regressions relating dry tissue weight of a standard individual as the de Zebra mussels are highly starvation tol pendent variable to days of starvation at 5°C (dot erant. Among starving N.A. mussels, 50% dashed line), 15°C (dashed line) and 25°C (solid line) mortalities (LT50) occurred after 118 days at (after Chase and McMahon, 1995). 25°C and 352 days at 15°C, corresponding 100% mortalities (SM100) occurring at 143 and 545 days, respectively (Chase and Mc Dry shell mass in a 20 mm SL standard Mahon, 1995). A 67% mortality occurred specimen remained constant during pro after 774 days starvation at 5°C (R. Chase, longed starvation at 25°C, but declined at personal communication). Estimated for a 5°C and increased at 15°C (Chase and Mc 20 mm shell length (SL) standard individ Mahon, 1995). Shell mass increase at 15°C ual, dry tissue mass loss at death was 74% was likely due to nacre deposition without at 25°C and 69% at 15°C (Chase and Mc corresponding increase in shell length while Mahon, 1995), similar to a 76% loss re decrease in shell mass at 5°C was likely due ported for European mussels on a submain to dissolution of shell mineral components tenance ration for 700 days at 4.5-5.5°C at greater rates than metabolic capacity for (Walz, 1978c). Similar levels of starvation secretion (Chase and McMahon, 1995). tolerance and dry tissue mass loss have During the first 10 days of a 31 day star been reported for C. fluminea (Cleland et vation period, tissue mass reduction was al., 1986). Mussel dry tissue weight de greatest in the digestive diverticula of zebra creased linearly with time of starvation, mussels. Thereafter, gonadal degradation loss rate increasing with increased temper accounted for the majority of weight loss ature (Fig. 8). Based on tissue energy con (Sprung and Borcherding, 1991). In starv tent, metabolic rates of starving mussels ing mussels, tubules of the digestive diver were 22%, 11% and 10% those of fed in ticulum either condensed or degraded com dividuals at 25°C, 15° and 5°C, respectively pletely. Gonads of starving individuals may (Chase and McMahon, 1995). In contrast, degenerate with gametes being reabsorbed. Vo2 was not reduced in European mussels Gonad degeneration was more pronounced during a much shorter, 31 day starvation pe in post-reproductive individuals than in re riod (Sprung and Borcherding, 1991). Met productive individuals (Bielefeld, 1991). abolic depression during prolonged starva Even after starvation for up to 21 days at tion, particularly at low temperatures 20°C, N.A. zebra mussels could still be in (^5°C), could allow mussels to overwinter duced to spawn by external seratonin ap without significant loss of reproductive en plication (Fong et al., 1996). In nonstarved ergy stores (Chase and McMahon, 1995). mussels, carbohydrates made up <11% and 354 ROBERT F. MCMAHON lipids <18% of total dry tissue mass. Lipid 8.5 mg C liter"1. Pseudofeces were first pro stores were depleted during the first seven duced at 0.2 mg C liter"'. Pseudofeces pro days of a 31 day starvation period, while duction rate increased with further increase carbohydrate content remained stable. in algal concentration such that it remained Thus, the majority of maintenance energy constant at 67% of filtered algal carbon during the latter stages of starvation was above a ration of 2 mg C liter"1. Consump derived from protein catabolism (Sprung tion rate for a 40 mg C mussel at 15°C and Borcherding, 1991) which, in nonstar peaked at 75 u,g C hr"1 (=1.9 u>g algal C ved individuals, makes up 62% of dry tis mg"1 hr"1), decreasing at higher or lower sue mass (Walz, 1979). algal concentrations. Assimilation efficien Algal food concentrations required to cy [(assimilation rate/ingestion rate)(100)] prevent tissue loss (i.e., maintenance ra was 40.7% in terms of algal organic carbon tions) range from 0.1-0.3 mg C liter"1 (i.e., or 35.2% in terms of total algal organic mg algal organic carbon/liter) in 1 yr old, mass. This value falls within that reported and 0.1-0.7 mg C liter"1 in 2 yr old mussels for other freshwater molluscs (Aldridge, at 4°-18°C (Walz, 1978c). Maintenance ra 1983; Burky, 1983; McMahon, 19836) and tions increase with increasing temperature is bracketed by summer and fall assimila (Walz, 19786) as metabolic demands in tion efficiencies of 6—95% recorded for a crease (Fig. 3). Major reductions in tissue Polish zebra mussel population (Stanczy protein content (=67%) occurred in mus kowska, 1977). sels fed submaintenance rations for 700 Ration, temperature and body size effect days (Walz, 1978c). Above 20°C, elevated zebra mussel tissue growth rates (Walz, metabolic demands (Fig. 3) cause mainte 19786). Maximum gross growth efficien nance rations to exceed maximal assimila cies [(tissue growth rate/consumption tion rates, leading to loss of tissue and pro rate)(100)] of =60% occurred at moderate tein mass (Walz, 19786). Inability to sup levels of consumption (algal carbon con port maintenance demands above 20°C sumption = 1-2% of mussel tissue carbon may, in part, cause the tissue mass reduc mass/d) at 8-10°C. It declined at higher tions reported among zebra mussels during temperatures and greater ration levels. As summer months (see section on Tempera similation efficiencies were essentially sim ture Responses) and suggests that mussel ilar over a wide size range and across 8°C maintenance above 20°C could cause rapid to 20°C (Table 2; Walz, 19786). Smaller physiological deterioration. mussels allocated greater assimilation to D. polymorpha veliger larvae feed on al growth, particularly at elevated tempera gal particles 1—4 jim in diameter and may tures. Larger individuals (i.e., 20 or 40 mg starve when phytoplankton is dominated by total tissue C) had no or negative growth at larger or smaller algal species (Sprung, 20°C as maintenance demands approached 1989). Starving veligers generally continue or surpassed assimilation rates (Table 2; to swim, experiencing 100% mortality Walz 19786). The percentage of assimilated within 11-15 days at 12°-24°C (Sprung, carbon allocated to tissue growth in smaller 1989). individuals (i.e., 5 and 20 mg tissue C) at <15°C (range = 30.8-71.5%) was high BlOENERGETICS compared to other freshwater bivalves Studies of bioenergetics have only been (Burky, 1983; McMahon, 1991), account published for European zebra mussel pop ing for the rapid growth of juvenile and ulations, although several N.A. studies were subadult mussels below 20°C. In contrast, in progress at the writing of this article. reduced carbon allocation to growth in larg Walz (1978a) showed that filtration rates re er mussels (>20-40 mg tissue C) may ac mained constant in media with algal con count for their low growth rates (Walz, centrations up to 2 mg C liter"1 (i.e., mg 19786 and references therein). Lack of tis algal organic carbon/liter), but proportion sue growth in larger mussels above 20°C ately declined at higher concentrations such needs further confirmation because N.A. ze that consumption rate was constant over 2 bra mussels sustain substantial summer PHYSIOLOGICAL ECOLOGY OF ZEBRA MUSSELS 355 growth in Lake Erie (Griffiths et al., 1991) and the lower Mississippi Rive (Tr . H. 1 °o 5 — # •* Diet z, personacommunicati l on) where wa S 6 — o o 1 O rn ^ S ters are >20°C throughou t the s ummer. a — I Thu s the, y appe ar to be acc umulating new -S tissu e mas sat t emperatures well ab ove the u •S so uppe r 20°C thr eshold for m aintenanc e of E tissu e growth in European mussels. a o tn * o — o — e i v- High growth rate sand s hort life spans o allow zebra mussels to rapidly reach high E -< densities in favorable habitats (Claudi and 00 W^ ^Q ^C) O S^ .o M O 8= Mackie, 1993). Capacity for population c °=0 vo in t-; rn _ rn NO growth is measured by P/B ratios (i.e., an d —' in •*' d d ON nual productivity rate/average standing crop biomass) equivalent to the fraction of pop ulation standing crop biomass produced an- 3 ° 00 — ^ I" 20 • t issue O tN o\ O greater than that of 0.2 determined for the tividu vo n t inc tal long-lived unionid, Anodonta anatina (L.) t (Negus, 1966). Low P/B values suggest that u O 6s ,s ^ Polish populations were slow growing and in o\ 8s 8s m O # E — O\ — O\ o r— Species Life cycle stage Environmental tolerance limits Temperature tolerance D. polymorpha Adult Cannot survive above 30°C Veliger larva Fertilizaton, 10°-26°C; Development 12°-24°C D. bugensis Adult Unknown, upper limit likely < D. polymorpha Veliger larva Unknown Respiratory response D. polymorpha Adult O2 uptake rate maximized at 3O-35°C Veliger larva Unknown, requires further study D. bugensis Adult Unknown, requires further study Veliger larva Unknown, requires further study Anoxia/hypoxia tolerance D. polymorpha Adult PO2 a 32-40 torr at 25°C, poor O2 regulator Veliger larva PO2 > 32 torr at 18-20°C D. bugensis Adult Unknown, likely > tolerance than D. polymorpha Veliger larva Unknown, requires further study 50 O Salinity tolerance D. polymorpha Adult Variable, <4-8%o, may acclimatize to higher levels » Veliger larva <7%o for spawning, <6%o for development m D. bugensis Adult <4%o, requires further study 3 Veliger larva <4%o, requires further study Emersion tolerance D. polymorpha Adult Dependent on temp, and R.H., <8 days above 25° Veliger larva Unknown, likely to be highly intolerant s D. bugensis Adult Similar to D. polymorpha, reduced at high R.H. Veliger larva Unknown, likely to be highly intolerant Freezing air temperature tolerance D. polymorpha Adult Single mussels < -1.5°C, when clustered < -3.0°C Veliger larva Unknown, likely to be highly intolerant D. bugensis Adult Unknown, likely £ than that of D. polymorpha Veliger larva Unknown, likely to be highly intolerant Ph limits D. polymorpha Adult £6.5, >8 for maximal growth Veliger larva 7.4-9.4 for successful development, optimum = 8.4 D. bugensis Adult Unknown, requires study Veliger larva Unknown, requires study Calcium concentration limits D. polymorpha Adult lower limit = 15 mg/1, a 25 mg/1 for good growth Veliger larva lower limit = 12 mg/1, optimum £34 mg/1 D. bugensis Adult Unknown, requires study Veliger larva Unknown, requires study Starvation tolerance D. polymorpha Adult LT50 = 118 d at 25°, 352 d at 15°, >500 d at 5°C Veliger larva 100% mortality in 11-15 days at 12°-24°C D. bugensis Adult Unknown, requires study Veliger larva Unknown, requires study PHYSIOLOGICAL ECOLOGY OF ZEBRA MUSSELS 357 ergy demands are similar in zebra mussels regardless of reproductive state (Sprung, 1991). Instead, reduction in tissue mass during spawning is indicative of diversion of a large proportion of nonrespired assim i 1 ilation away from tissue growth into ga o o metogenesis. Reproductive costs require C w further assessment in N.A. and European ° 2 mussels. i i The short life-spans, early maturity, H -o « small gametes, high fecundities, and rapid z § £ growth rates of zebra mussels are life his O i '3 A T3T3T3 O.T3-OT3 • Ji T3 T3 tory characteristics associated with adapta r232i-233 g tag tion to unstable habitats where unpredicta r M i/i ui "Z3 w « w is.Sww ble environmental disturbance results in pe gssa *ass Seas riodic massive population reductions (Mc •^ '5 '3 '3 o '3 '3 '3 "CL. Z '3 '3 Mahon, 1991). These characteristics allow Etro-cr c o- o* o* ,, e a1 a" D. polymorpha to reach high densities rap w Ufc-fc- (j L u* u *-•-*• 1. u» ECCC T3CCC 3| C C idly after introduction to a favorable habitat 2SJ8 >,5^ c-** or recolonization of an unstable habitat O.^J<:UECEuEE^ c ^ ^ E ^ ±»C5,-^: C^( D.CCC UCC C — ^TCC from which they were extirpated by envi DDD3 QPDP VOD ronmental disturbance. CONCLUSIONS On the whole, there is general European and N.A. agreement on the resistance and capacity adaptations of D. polymorpha Qi}<-= Ofi --^ &)•= bfi — 00 — 00 (summarized in Table 3). Temperatures of ^-3 .^ 3^3 ^ 3^:3'^ initial and maximal spawning, respiratory responses, seasonal respiratory variation, responses to anoxia/hypoxia, salinity limits, calcium concentration limits, pH limits, and responses to starvation are relatively similar • o« a •ac among N.A. and European mussels, indic £• os- 0 o ative of a single species. Discrepancies re main in European and N.A. data regarding Iym Iym gen gen iym 0 3 ao. s a. - Q ao. temperature effects on growth rate and ther Ci Ci mal tolerance limits. Maximal growth rates of northern European populations occur at much lower temperatures (10°-15°C, Walz, 1978ft) than in Lake Erie (Griffiths et al, 1991) or the lower Mississippi River (T. H. Dietz, personal communication). Chronic upper thermal tolerance limits determined for northern European mussels are 27-28°C while they are 3O°-31°C among N.A. mus sels (McMahon et al, 1993, 1994). How ever, other European studies suggest the ze c bra mussel's thermal tolerance limits are h. similar to that of N.A. mussels (Tourari et al, 1988). Differences are likely to result from either genetic variation and/or non- genetic, ecophenotypic differences induced 358 ROBERT F. MCMAHON by differences in populations' thermal re of European and N.A. mussels; effects of gimes. pH and calcium concentration; respiratory Evidence exists for both hypotheses. and protein/nonprotein catabolic responses North American zebra mussels probably to season and long-term starvation; and bio originated from the northern shore of the energetic analyses of fast growing, highly Black Sea, the warmest region of this spe productive N.A. populations, particularly cies' European range. Thus, they may have with regard to reproductive costs and tem evolved greater thermal tolerance than mus peratures of optimal energetic efficiency sels from the colder northern waters on relative to European populations (Walz, which European physiological studies of 1978a, b, c). Physiological studies at all mussels have almost exclusively centered. levels are required for D. bugensis, for Conversely, the thermal tolerance limits of which little data presently exist (Table 3). N.A. mussels appear to be positively cor This species may be replacing D. polymor related with ambient water temperature pha in some N.A. habitats {e.g., Lake On even after laboratory temperature acclima tario and the St. Lawrence River). Knowl tion. This result suggests that differences in edge of its physiological responses is need thermal tolerance and temperature/growth ed to predict its eventual N.A. distribution. responses in N.A. and northern European This review indicates that D. polymorpha mussels may result from ecophenotypic is relatively less tolerant of environmental seasonal acclimatization of N.A. mussels to stress (Table 3) and a poorer hyperosmotic higher average abient water temperatures. regulator compared to native N.A. sphaeriid Elucidation of the bases for variation in the and unionid bivalves (Dietz et al, 1996). In thermal responses of N.A. and European this regard, it is similar to the nonindigen mussels will require rigidly controlled, ous, freshwater Asian clam, Corbicula flu comparative isozyme and/or DNA analyses minea (McMahon, 1991). Dreissena and of interpopulation genetic variation. Diver Corbicula are both heterodont bivalves rel gence of the population genetics of northern atively recently evolved from marine an European and Black Sea region mussels cestors, Dreissena, inhabiting freshwater and genetic similarity between Black Sea since the late Miocene (~13 106 yr, Nuttall, region and N.A. mussels would strongly 1990) and Corbicula, since the late Creta support a genetic basis for thermal response ceous (-70 106 yr, Keen and Casey, 1969). differences in northern European and N.A. In contrast, the super family, Unionacea, mussels. In contrast, lack of genetic diver has occupied freshwater since the Triassic gence would support nongenetic, seasonal (-245 106 yr, Haas, 1969) and the family, temperature acclimatization as of the basis Sphaeriidae, since the upper Jurassic (—150 for these differences. 106 yr, Dance, 1969). With much longer Comparative studies of European and freshwater histories, unionaceans and N.A. zebra mussel thermal responses sphaeriids appear to have become better should be carried out with the same exper adapted to the stresses of freshwater life imental protocols or within the same labo than either Corbicula or Dreissena. Mc ratories, assuring that differences do not re Mahon (1991) has argued that unionaceans sult from varying methodologies. Re and sphaeriids display life history charac sponses could also be studied in mussels teristics adapting them for life in stable, reciprocally transferred between European predictable habitats including: long life and N.A. populations for long enough to spans, extensive iteroparity, low effective allow acclimatization to local conditions. fecundities, large offspring, delayed matu Thus, intercontinental, collaborative, stud rity, and reduced growth rates. These traits ies should be of high priority in future zebra prevent both groups from rapid habitat re mussel physiological research. Other areas colonization after extirpation by environ of potentially valuable physiological re mental disturbance; thus, they have evolved search include: effects of seasonal accli extensive resistance adaptations that allow matization and geographic distribution on survival of environmental extremes. physiological variables; salinity tolerance Dreissenids and corbiculaceans, as rela PHYSIOLOGICAL ECOLOGY OF ZEBRA MUSSELS 359 tively recent colonizers of freshwaters, re fecundity, and bioenergetics in a natural popula tain some of the primitive characteristics of tion of the Asiatic freshwater clam, Corbicula manilensis Philippi, from north central Texas. J. their marine ancestors including planktonic Moll. Stud. 44:49-70. larvae, and reduced resistance to environ Alexander, J. E., Jr., J. H. Thorp, and R. D. Fell. 1994. mental stress. Poor stress tolerance makes Turbidity and temperature effects on oxygen con them less competitive than sphaeriids and sumption in the zebra mussel (Dreissena poly unionaceans in stable habitats (exception is morpha). Can. J. Fish. Aquat. Sci. 51:179-184. Alimov, A. F. 1975. The rate of metabolism in fresh zebra mussel colonization of unionacean water bivalve molluscs. Soviet J. Ecol. 5:6-13. shells). Instead, they have become special Alyakrinskaya, I. O. 1978. Biochemical adaptations ized for life in unstable habitats, their to drying conditions in bivalves in the Kruski Za planktonic larvae, elevated fecundity, fast liv Baltic Sea USSR. Zool. Zh. 57:136-138. growth, early maturity, and attenuated life- Bayne, B. L. 1973. Physiological changes in Mytilus edulis L. induced by temperature and nutritive spans allowing rapid reinvasion and reco stress. J. Mar. Biol. Ass. U.K. 53:39-58. lonization of unstable habitats after extir Bielefeld, U. 1991. Histological observation of go pation by unpredictable environmental dis nads and digestive gland in starving Dreissena turbance. In unstable habitats, selection polymorpha (Bivalvia). Malacologia 33:31-42. pressures for resistance or capacity adapta Birger, T. I., A. Ya. Malarevskaja, O. M. Arsan, V. D. Solomatina, and Yu. M. Gupalo. 1978. Physio tions are reduced, as they will not prevent logical aspects of adaptations of mollusks to abi extirpation by periodic massive disturbance. otic and biotic factors due to blue-green algae. Adaptation to unstable habitats and lack of Malacol. Rev. 11:100-102. natural biotic checks have allowed D. poly Borcherding, J. 1991. The annual reproductive cycle morpha and C. fluminea to be extremely of the freshwater mussel Dreissena polymorpha successful invaders of N.A. freshwaters. Pallas in lakes. Oecologia 87:208-218. Burky, A. J. 1983. Physiological ecology of fresh They have also made them of the most eco water bivalves. In W. D. Russell-Hunter (ed.), The nomically damaging aquatic species ever Mollusca, Vol. 6, Ecology, pp. 281-327. Academ introduced to North American freshwaters ic Press, Inc., Orlando, Florida. (McMahon, 1983a, 1991; Claudi and Byrne, R. A. and R. F. McMahon. 1994. Behavioral Mackie, 1993). and physiological responses to emersion in fresh water bivalves. Amer. Zool. 34:194-204. Chase, R. and R. F. McMahon. 1995. Starvation tol ACKNOWLEDGMENTS erance of zebra mussels, Dreissena polymorpha. In Proceedings of the fifth international zebra My physiological research on Dreissena mussel and other aquatic nuisance species con polymorpha is supported by grants from the ference 1995, pp. 31-38. Ontario Hydro, Toronto, U.S. Army, Corps of Engineers, Waterways Ontario. Experiment Station and the U.S. Army Of Clarke, M. 1993. Freeze sensitivity of the zebra mus fice of Research. My collaborators include: sel (Dreissena polymorpha) with reference to de watering during freezing conditions as a mitiga James E. Alexander, Jr.; Thomas H. Dietz; tion strategy. Masters Thesis, The University of Paul D. Johnson; Roger A. Byrne; Law Texas at Arlington, Arlington, Texas. rence R. Shaffer; Neal J. Smatresk; Mark Clarke, M., R. F McMahon, A. C. Miller, and B. S. L. Burleson, Michael Clarke, Ricki A. Payne. 1993. Tissue freezing points and time for Chase, Michael R. Hernandez, Jeffrey Nel complete mortality on exposure to freezing air son and Thomas A. Ussery. temperatures in the zebra mussel (Dreissena poly morpha) with special reference to dewatering dur ing freezing conditions as a mitigation strategy. In REFERENCES J. L. Tsou and Y. G. Mussalli (eds.), Proceedings, Afanas'yev, S. A. and A. A. Protasov. 1987. Char third international zebra mussel conference, 1993, acteristics of a Dreissena population in the pe pp. 4-120-4-145. 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