Influence of Hydrologic Processes on Reproduction of the Introduced Bivalve Potamocorbzch amzcrensis

in Northern San Francisco Bay, California1

Francis Parchaso and Janet K. Thompson2

Abstract: Monthly censusing of reproductive condition of the Asian clam Pota-mocorbula amurensis at four sites in northern San Francisco Bay over a 9-yr pe- riod revealed year-to-year differences in local reproductive activity that are associated with patterns of hydrologic variability. Between 1989 and 1992, Northern California experienced a drought, whereas the period between 1993 and 1998 was marked by a mix of wet and dry years. We took advantage of the extreme year-to-year differences to examine reproductive responses to river in- flow patterns. Populations of P. amurensis at the upstream sites in Suisun Bay and Carquinez Strait were more reproductively active during wet years than dry years. Conversely, at the downstream site in San Pablo Bay, the population was more reproductively active during dry years than wet years. We suggest that the different reproductive patterns observed reflect the clam's response to different sources of food. During wet years, organic matter from the rivers augments food supplies in Suisun Bay. During dry years, when inflow into the San Francisco Bay Estuary from the rivers is reduced, water transported from the adjacent ocean into the estuary as far as San Pablo Bay provides a supplemental food supply for the local production. The populations take advantage of these spa- tially distinct food supplies by initiating and maintaining local reproductive activity. We conclude that the ability of P. amurensis to consume and use various types of food to regulate its reproductive activity is part of the reason for its success as an invasive species.

THEASIAN cLAM Potamocorbula amurensis, a exotic species introductions in estuaries, and native of East Asia, Khabarovsk (a republic of in San Francisco Bay in particular (Cohen the former Soviet Union), and Korea, was and Carlton 1998), the mechanisms of the introduced into San Francisco Bay in 1986. successful spread of a species following inoc- The success with which P. amurensis colo- ulation is of growing interest. In a 2-yr period nized and established itself in the benthic com- (1 986- 1987) P. amurensis spread throughout munity of San Francisco Bay has been well San Francisco Bay, occupying a variety of in- documented (Thompson et al. 1988, Carlton tertidal and subtidal substrates (sand, clay, et al. 1990, Nichols et al. 1990), although the mud, peat, and combinations thereof) in a reasons for its success have not been dis- wide range of salinities (1 to >30 psu) (Carl- cussed. In this period of accelerating rates of ton et al. 1990). The spatial success of P.

amurensis is acutely relevant in this estuary because P. amurensis is an efficient filter feeder, ' Support for this project was provided by the San able to filter food ranging in size from bacte-

Francisco Bay Toxic Substances Hydrology Program and the San Francisco Bay Place-Based Ecosystem Program. ria to copepod larvae (Werner and Holli- Manuscript accepted 28 November 2001. baugh 1993, l m m e r e r et al. 1994). Several

* U.S. Geological Survey, Water Resources Division, authors (Cloern 1982, Nichols 1985) have Menlo Park, California 94025. suggested mechanisms by which the filter-

feeding benthos, primarily bivalves, can con- Pacific Science (2002), vol. 56, no. 3:329-345 trol phytoplankton biomass in both South 02002 by University of Hawai'i Press and North San Francisco Bay, and Alpine and All rights reserved Cloern (1 992) hypothesized that P. amurensis

Influence of Hydrologic Processes on Reproductionof the Introduced Bivalve Potamocorbula amurensis

in Northern San Francisco Bay, California!

Francis Parchaso and Janet K. Thompson2

Abstract: Monthly censusing of reproductive condition of the Asian clam Pota­mocorbula amurensis at four sites in northern San Francisco Bay over a 9-yr pe­riod revealed year-to-year differences in local reproductive activity that areassociated with patterns of hydrologic variability. Between 1989 and 1992,Northern California experienced a drought, whereas the period between 1993and 1998 was marked by a mix of wet and dry years. We took advantage of theextreme year-to-year differences to examine reproductive responses to river in­flow patterns. Populations of P. amurensis at the upstream sites in Suisun Bayand Carquinez Strait were more reproductively active during wet years than dryyears. Conversely, at the downstream site in San Pablo Bay, the population wasmore reproductively active during dry years than wet years. We suggest that thedifferent reproductive patterns observed reflect the clam's response to differentsources of food. During wet years, organic matter from the rivers augments foodsupplies in Suisun Bay. During dry years, when inflow into the San FranciscoBay Estuary from the rivers is reduced, water transported from the adjacentocean into the estuary as far as San Pablo Bay provides a supplemental foodsupply for the local production. The populations take advantage of these spa­tially distinct food supplies by initiating and maintaining local reproductiveactivity. We conclude that the ability of P. amurensis to consume and use varioustypes of food. to r~gulate .its reproductive activity is part of the reason for itssuccess as an InVaSIVe specIes.

THE ASIAN CLAM Potamocorbula amurensis, anative of East Asia, Khabarovsk (a republic ofthe former Soviet Union), and Korea, wasintroduced into San Francisco Bay in 1986.The success with which P. amurensis colo­nized and established itself in the benthic com­munity of San Francisco Bay has been welldocumented (Thompson et al. 1988, Carltonet al. 1990, Nichols et al. 1990), although thereasons for its success have not been dis­cussed. In this period of accelerating rates of

I Support for this project was provided by the SanFrancisco Bay Toxic Substances Hydrology Program andthe San Francisco Bay Place-Based Ecosystem Program.Manuscript accepted 28 November 2001.

2 U.S. Geological Survey, Water Resources Division,Menlo Park, California 94025.

Pacific Science (2002), vol. 56, no. 3:329-345© 2002 by University of Hawai'i PressAll rights reserved

exotic species introductions in estuaries, andin San Francisco Bay in particular (Cohenand Carlton 1998), the mechanisms of thesuccessful spread of a species following inoc­ulation is of growing interest. In a 2-yr period(1986-1987) P. amurensis spread throughoutSan Francisco Bay, occupying a variety of in­tertidal and subtidal substrates (sand, clay,mud, peat, and combinations thereof) in awide range of salinities (1 to >30 psu) (Carl­ton et al. 1990). The spatial success of P.amurensis is acutely relevant in this estuarybecause P. amurensis is an efficient filter feeder,able to filter food ranging in size from bacte­ria to copepod larvae (Werner and Holli­baugh 1993, Kimmerer et al. 1994). Severalauthors (Cloern 1982, Nichols 1985) havesuggested mechanisms by which the filter­feeding benthos, primarily bivalves, can con­trol phytoplankton biomass in both Southand North San Francisco Bay, and Alpine andCloern (1992) hypothesized that P. amurensis

329

is responsible for the disappearance of the annual phytoplankton bloom in the northern bay. The continuing dominance of P. amur­ensis in San Francisco Bay has also resulted in changes in the San Francisco Bay ecosystem by altering both benthic community structure and interspecific dynamics (Nichols et al. 1990).

An important component in the spatially extensive success of P. amul-ensis is its ability to reproduce and recruit into established benthic communities under highly variable conditions characteristic of the estuarine en- vironment. In this study, we examined con- nections between patterns of change in the estuary's hydrologic regime and the repro- ductive patterns of P. amurensis during a 9-yr period at four sites along the salinity gradient in northern San Francisco Bay. We show that P. amurensis successfully reproduces in north- ern San Francisco Bay every year, and that

PACIFIC SCIENCE . July 2002

local reproductive patterns within each year are related to spatial and temporal changes in the hydrologic conditions and thus in the food supply along the salinity gradient of the estuary. The success of P. amurensis in this system is therefore related to its ability to use a variety of food sources and the apparent lack of temperature or salinity control on repro- ductive activity.

Hydrologic Setting

The drainage basin of the Sacramento-San Joaquin River system (Figure 1) is the source of 90% of the freshwater inflow into San Francisco Bay (Conomos et al. 1985). Fresh- water flow within this river-estuary system, although managed by dams and diversions, is seasonal, composed of rainfall runoff in the winter and snowmelt in the spring and early summer. The adjacent Pacific Ocean is the

FIGUREI. Freshwater flow from the drainage basin of the Sacramento and San Joaquin Rivers into San Francisco Bay. Inset shows study area.

330 PACIFIC SCIENCE· July 2002

is responsible for the disappearance of theannual phytoplankton bloom in the northernbay. The continuing dominance of P. amur­ensis in San Francisco Bay has also resulted inchanges in the San Francisco Bay ecosystemby altering both benthic community structureand interspecific dynamics (Nichols et al.1990).

An important component in the spatiallyextensive success of P. amurensis is its abilityto reproduce and recruit into establishedbenthic communities under highly variableconditions characteristic of the estuarine en­vironment. In this study, we examined con­nections between patterns of change in theestuary's hydrologic regime and the repro­ductive patterns of P. amurensis during a 9-yrperiod at four sites along the salinity gradientin northern San Francisco Bay. We show thatP. amurensis successfully reproduces in north­ern San Francisco Bay every year, and that

local reproductive patterns within each yearare related to spatial and temporal changes inthe hydrologic conditions and thus in thefood supply along the salinity gradient of theestuary. The success of P. amurensis in thissystem is therefore related to its ability to usea variety of food sources and the apparent lackof temperature or salinity control on repro­ductive activity.

Hydrologic Setting

The drainage basin of the Sacramento-SanJoaquin River system (Figure 1) is the sourceof 90% of the freshwater inflow into SanFrancisco Bay (Conomos et al. 1985). Fresh­water flow within this river-estuary system,although managed by dams and diversions, isseasonal, composed of rainfall runoff in thewinter and snowmelt in the spring and earlysummer. The adjacent Pacific Ocean is the

600000 l

500000

400000

,-..,

~u-; 300000o~

200000

100000

19971996199519941993199219911990

o ~-'lIlIIW'lol~IIM_~'-""""IL~_~-----!''''''~~~------''

1989

FIGURE 1. Freshwater flow from the drainage basin of the Sacramento and San Joaquin Rivers into San Francisco Bay.Inset shows study area.

Influence of Hydrologic Processes on Potarnocoldula amur.ensis . Parchnso and Thompson

FIGURE2. Northern San Francisco Bay and Sacramento and San Joaquin River Delta showing collection sites in cen- tral San Pablo Bay, Carquinez Strait, and Suisun Bay. All stations are located in the deep-water shipping channel.

source of saline water that is transported tidally into San Francisco Bay through the Golden Gate (Figure 2). The extent of the marine influence on the salinity gradient within San Francisco Bay is hghly seasonal. In dry summers, saline water can reach as far as the confluence of the Sacramento and San Joaquin Rivers. During extremely wet winters low-salinity water (<lo psu) can be found throughout northern San Francisco Bay and beyond the Golden Gate (Conomos et al. 1985).

During this study, California experienced a 6-yr drought that ended in 1993 (Figure 1). The following year, 1994, was also a dry year. The California Department of Water Re­sources classified the remaining years of this study (1995-1997) as wet years. The differing hydrologic conditions during this study pro- vide a contrast in environmental influences

that coincide with changes in the reproduc- tive behavior of P. amurensis.

Bivalve Reproductive Strategies

Giese and Pearse (1974, 1979), in their review of reproduction in bivalves, described many exogenous regulators of gametogenesis. As an example, they pointed out that it is important that marine invertebrates reproduce at a time when the young have a good chance of sur- viving (e.g., when temperatures, salinity, or food conditions are favorable for larval sur- vival). Often, reproductive activities such as gametogenesis are begun much in advance of such favorable conditions, indicating that some environmental changes must act as early cues to synchronize reproduction with the subsequent favorable conditions. These en­vironmental changes represent an indirect

Influence of Hydrologic Processes on Potamocorbula amurensis . Parchaso and Thompson 331

San Pablo Bay

~• Carq"",e"J;,r:,

J San Pablo Bay

~ (SPB)

~Q~~ Cenrral Bay)

~>~ ~Pacific Ocean,f \ t~

San Francisco1,.t

o

o 10 kilometers

FIGURE 2. Northern San Francisco Bay and Sacramento and San]oaquin River Delta showing collection sites in cen­tral San Pablo Bay, Carquinez Strait, and Suisun Bay. All stations are located in the deep-water shipping channel.

source of saline water that is transportedtidally into San Francisco Bay through theGolden Gate (Figure 2). The extent of themarine influence on the salinity gradientwithin San Francisco Bay is highly seasonal.In dry summers, saline water can reach as faras the confluence of the Sacramento and SanJoaquin Rivers. During extremely wet winterslow-salinity water « 10 psu) can be foundthroughout northern San Francisco Bay andbeyond the Golden Gate (Conomos et al.1985).

During this study, California experienced a6-yr drought that ended in 1993 (Figure 1).The following year, 1994, was also a dry year.The California Department of Water Re­sources classified the remaining years of thisstudy (1995-1997) as wet years. The differinghydrologic conditions during this study pro­vide a contrast in environmental influences

that coincide with changes in the reproduc­tive behavior of P. amurensis.

Bivalve Reproductive Strategies

Giese and Pearse (1974, 1979), in their reviewof reproduction in bivalves, described manyexogenous regulators of gametogenesis. As anexample, they pointed out that it is importantthat marine invertebrates reproduce at a timewhen the young have a good chance of sur­viving (e.g., when temperatures, salinity, orfood conditions are favorable for larval sur­vival). Often, reproductive activities such asgametogenesis are begun much in advance ofsuch favorable conditions, indicating thatsome environmental changes must act as earlycues to synchronize reproduction with thesubsequent favorable conditions. These en­vironmental changes represent an indirect

332

exogenous control on reproduction. Such environmental changes need not be restricted to a single factor, but may consist of several factors that, when operating together, can externally stimulate synchrony of reproduc-tive activities.

Studies of the reproductive cycles of other introduced bivalves common in San Francisco Bay show that bay populations tend to have longer reproductive seasons than are reported for conspecific populations on the Atlantic and Pacific Northwest coast of North Arner-ica. For example, Rosenblum and Niesen (1985) found that Mya arenaria was repro-ductively active from March through No-vember in San Francisco Bay, a reproductive season 2 months longer than seen in pop-ulations in the state of Washington. Pacific

'2

coast populations of M. arenaria also have a single reproductive season, whereas Atlantic coast populations have a biannual reproduc-tive cycle. These differences in the reproduc-tive cycle of M. arenaria have been attributed to differences in temperature regimes: San Francisco Bay has a longer period of opti-mum temperatures than in Washington; fa-vorably warm temperatures occur initially between March and Aoril and secondarilv between June and ~ u l y 'on the East ~ o a & (Rosenblum and Niesen 1985).

Varon (1978) found a similarly long re-productive season in Venerupis japonia, a native of Japan, in San Francisco Bay (April through October), which is slightly longer than that of the same species in Washington (April through September). He also noted that populations in Japan have biannual spawns and suggested that the differing temperature regimes among the three locations may be responsible for their different reproductive patterns.

Previous studies of reoroduction in P. amurensis and congeneric species have de-scribed the reproductive behavior and sug-gested environmental factors that may influ-ence reproduction. In San Francisco Bay, Parchaso (1995) found that P. amurensis is di-oecious, begins reproducing at approximately 4 mm in l e n d . and has both seasonal re-

' 2 ,

production in Suisun Bay and near-continu-ous reproduction in South San Francisco Bay. Furthermore, temperature and salinity

PACIFIC SCIENCE . July 2002

changes were not controlling factors of re-production. That earlier work was con-ducted during the previously mentioned 6-yr drought.

Carlton et al. (1990) reviewed reproduc-tion literature for a congeneric species in Asia, Potarnocorbula laevis, and found that this species undergoes gametogenesis between mid-September and mid-October when water temperature is between 12 and 23°C. Pota-mocorbula laevis is primarily dioecious, with a few hermaphrodites observed. Fertile eggs are released when water temperature is be-tween 16 and 20°C. Metamorphosis to a ve-liger larva occurs after 20 to 22 days, and settlement occurs after 30 to 40 days a t a size of 370 pm.

Study Locations

Northern San Francisco Bay is a partially mixed estuary dominated by seasonally vary-ing river flow from the Sacramento and San Joaquin Rivers, which are fed by numerous tributary rivers and streams that drain the Sierra Nevada Range (Figure 1). Our four sampling sites are located in three different regions along the salinity gradient of the northern San Francisco Bay estuary: (1) Sui-sun Bay, (2) Carquinez Strait, connecting San Pablo Bay and Suisun Bay, and (3) San Pablo Bay (Figure 2). These regions were selected to represent different environmental charac-teristics, each with distinct patterns of varia-tion in physical characteristics (e.g., tempera-ture and salinity) at the sites.

The Mallard Island station (MI) is located near the confluence of the Sacramento and San Joaquin Rivers (Figure 2). During the winter and spring, salinities can be as low as 0 psu and temperatures can be as low as 4°C. During the summer and fall, salinities range from 10 to 15 psu and temperatures can reach 23'C (Conomos 1979, Cloern and Nichols 1985).

The Concord Naval Weapons Station (CNWS) site is located north of the Concord Naval Weapons Station in the southern part of Suisun Bay and in the deep-water shipping channel (Figure 2). The salinity and temper-ature characteristics are similar to those at MI.

332

exogenous control on reproduction. Suchenvironmental changes need not be restrictedto a single factor, but may consist of severalfactors that, when operating together, canexternally stimulate synchrony of reproduc­tive activities.

Studies of the reproductive cycles of otherintroduced bivalves common in San FranciscoBay show that bay populations tend to havelonger reproductive seasons than are reportedfor conspecific populations on the Atlanticand Pacific Northwest coast of North Amer­ica. For example, Rosenblum and Niesen(1985) found that Mya arenaria was repro­ductively active from March through No­vember in San Francisco Bay, a reproductiveseason 2 months longer than seen in pop­ulations in the state of Washington. Pacificcoast populations of M. arenaria also have asingle reproductive season, whereas Atlanticcoast populations have a biannual reproduc­tive cycle. These differences in the reproduc­tive cycle of M. arenaria have been attributedto differences in temperature regimes: SanFrancisco Bay has a longer period of opti­mum temperatures than in Washington; fa­vorably warm temperatures occur initiallybetween March and April and secondarilybetween June and July on the East Coast(Rosenblum and Niesen 1985).

Varon (1978) found a similarly long re­productive season in Venerupis japonica, anative of Japan, in San Francisco Bay (Aprilthrough October), which is slightly longerthan that of the same species in Washington(April through September). He also noted thatpopulations in Japan have biannual spawnsand suggested that the differing temperatureregimes among the three locations may beresponsible for their different reproductivepatterns.

Previous studies of reproduction in P.amurensis and congeneric species have de­scribed the reproductive behavior and sug­gested environmental factors that may influ­ence reproduction. In San Francisco Bay,Parchaso (1995) found that P. amurensis is di­oecious, begins reproducing at approximately4 mm in length, and has both seasonal re­production in Suisun Bay and near-continu­ous reproduction in South San FranciscoBay. Furthermore, temperature and salinity

PACIFIC SCIENCE· July 2002

changes were not controlling factors of re­production. That earlier work was con­ducted during the previously mentioned 6-yrdrought.

Carlton et al. (1990) reviewed reproduc­tion literature for a congeneric species inAsia, Potamocorbula laevis, and found that thisspecies undergoes gametogenesis betweenmid-September and mid-October when watertemperature is between 12 and n°c. Pota­mocorbula laevis is primarily dioecious, with afew hermaphrodites observed. Fertile eggsare released when water temperature is be­tween 16 and 20°C. Metamorphosis to a ve­liger larva occurs after 20 to 22 days, andsettlement occurs after 30 to 40 days at a sizeof 370 J.lm.

Study Locations

Northern San Francisco Bay is a partiallymixed estuary dominated by seasonally vary­ing river flow from the Sacramento and SanJoaquin Rivers, which are fed by numeroustributary rivers and streams that drain theSierra Nevada Range (Figure 1). Our foursampling sites are located in three differentregions along the salinity gradient of thenorthern San Francisco Bay estuary: (1) Sui­sun Bay, (2) Carquinez Strait, connecting SanPablo Bay and Suisun Bay, and (3) San PabloBay (Figure 2). These regions were selectedto represent different environmental charac­teristics, each with distinct patterns of varia­tion in physical characteristics (e.g., tempera­ture and salinity) at the sites.

The Mallard Island station (MI) is locatednear the confluence of the Sacramento andSan Joaquin Rivers (Figure 2). During thewinter and spring, salinities can be as low aso psu and temperatures can be as low as4°C. During the summer and fall, salinitiesrange from 10 to 15 psu and temperatures canreach noc (Conomos 1979, Cloern andNichols 1985).

The Concord Naval Weapons Station(CNWS) site is located north of the ConcordNaval Weapons Station in the southern partof Suisun Bay and in the deep-water shippingchannel (Figure 2). The salinity and temper­ature characteristics are similar to those atMI.

333Influence of Hydro1og.i~Processes on Pota7nocorbirla a7nzcrensis . Pa~,chasoand Thowpson

The Carquinez Strait station (CS), located in the narrow channel that connects Suisun and San Pablo Bays (Figure 2), is charac-terized by high tidal current velocities and enhanced vertical tidal mixing (Walters et al. 1985). Carquinez Strait is a transitional zone between San Pablo Bay and Suisun Bay, with salinities rangmg from 2 psu in the winter to 15 psu in the summer (Conomos et al. 1985) and temperatures ranging between 10 and 20°C (Conomos 1979).

The San Pablo Bay site (SPB), in the large embayment west of Carquinez Strait, is lo-cated on the edge of the shipping channel east of Pt. Pinole (Figure 2). San Pablo Bay salin-ities range from 20-28 psu in the spring to 24-30 psu in the fall, and temperatures range from 8°C in the winter to 18'C in the sum-mer (Conomos et al. 1985). Seasonal fresh-water and marine influences characterizc the SPB site.

MATERIALS AND M E T H O D S

Potamocorbulu anzurensis specimens were col-lected monthly from the four subtidal sta-tions, from October 1989 to December 1997, to determine their reproductive condition. Clams were collected with a Van Veen grab (0.05 mZ)and preserved in 10% buffered for-malin. In the laboratory, 10 to 15 clams rep-resenting the full size range available at each station were examined for each sampling date. Minimum sample size was 10 except during months when tissue samples were damaged during the histological processing or when animals were difficult to collect.

The visceral mass of each clam was re-moved and stored in 70% ETOH. The tissues were prepared using standard histo-logical techniques. The embedded samples were thin sectioned using a microtome and then stained with Harris' hematoxylin and eosin. The stained thin sections were exam-ined with a light microscope. Each specimen was characterized by sex and developmental stage of the gonads, thus allowing each spec-imen to be placed in one of five qualitative stages of gonadal development: inactive, active, ripe, spawning, and spent.

Individuals at each reproductive stage at each station were tabulated and the data con-

verted to percentages. Although five gonadal stages were defined, gonadal development in many of the clams was continuous, and the clams were commonly in transition between stages (e.g., developing from active to ripe). T o alleviate the difficulty in determining the developmental stages of clams in transition between the defined stages, the percentages of clams in the active, ripe, and partially spent stages were given positive values (multiplied by +I), and the percentages of clams in the inactive and spent stages were given negative values (multiplied by -1). These values were summed for each month at each station, and these represent the "central tendency of re-production." For example: a month with 30% active, 10% ripe, and 70% inactive clams would be scored as -30%. A Kruskal-Wallis one-way analysis of variance (ANOVA) was used to test significance among the monthly central tendencies. The coefficient of varia-tion of each month was used to compare the variation in reproduction between wet and dry years.

T o characterize the physical and biological environment of northern San Francisco Bay during our study, we used temperature, sa-linity, and chlorophyll data collected by other agencies. The California Department of Water Resources (CDWR) collected Mallard Island and Carquinez Strait salinity and tem-perature data every hour using an in situ surface conductivity and temperature sensor (California Department of Water Resources 1999). San Pablo Bay data were collected every 15 min by the U.S. Geological Survey (USGS) using in situ conductivity and tem-perature sensors on the surface and bottom (Buchanan 1999). These salinity and temper-ature data were summarized to acquire a mean monthly value for wet and dry years. Chlorophyll a fluxwas calculated as described by Jassby et al. (1993): multiplication of the characteristic surface chlorophyll a concen-tration of the Sacramento and San Joaquin Rvers by their outflow rates. These values represent the estimated carbon from micro-algae that are transported into the bay from the freshwater tributaries. Because primary production can be high in these areas, the carbon flu%can be substantial (Jassby et al. 1993). Chlorophyll a concentrations for the

Influence of Hydrologic Processes on Potmnocorbula amurensis . Parchaso and Thompson 333

The Carquinez Strait station (CS), locatedin the narrow channel that connects Suisunand San Pablo Bays (Figure 2), is charac­terized by high tidal current velocities andenhanced vertical tidal mixing (Walters et a!'1985). Carquinez Strait is a transitional zonebetween San Pablo Bay and Suisun Bay, withsalinities ranging from 2 psu in the winter to15 psu in the summer (Conomos et a1. 1985)and temperatures ranging between 10 and20nC (Conomos 1979).

The San Pablo Bay site (SPB), in the largeembayment west of Carquinez Strait, is lo­cated on the edge of the shipping channel eastof Pt. Pinole (Figure 2). San Pablo Bay salin­ities range from 20-28 psu in the spring to24-30 psu in the fall, and temperatures rangefrom 8°C in the winter to 18°C in the sum­mer (Conomos et a1. 1985). Seasonal fresh­water and marine influences characterize theSPB site.

MATERIALS AND METHODS

Potamocorbula amurensis specimens were col­lected monthly from the four subtidal sta­tions, from October 1989 to December 1997,to determine their reproductive condition.Clams were collected with a Van Veen grab(0.05 m 2

) and preserved in 10% buffered for­malin. In the laboratory, 10 to 15 clams rep­resenting the full size range available at eachstation were examined for each sampling date.Minimum sample size was 10 except duringmonths when tissue samples were damagedduring the histological processing or whenanimals were difficult to collect.

The visceral mass of each clam was re­moved and stored in 70% ETOH. Thetissues were prepared using standard histo­logical techniques. The embedded sampleswere thin sectioned using a microtome andthen stained with Harris' hematoxylin andeosin. The stained thin sections were exam­ined with a light microscope. Each specimenwas characterized by sex and developmentalstage of the gonads, thus allowing each spec­imen to be placed in one of five qualitativestages of gonadal development: inactive, active,ripe, spawning, and spent.

Individuals at each reproductive stage ateach station were tabulated and the data con-

verted to percentages. Although five gonadalstages were defined, gonadal development inmany of the clams was continuous, and theclams were commonly in transition betweenstages (e.g., developing from active to ripe).To alleviate the difficulty in determining thedevelopmental stages of clams in transitionbetween the defined stages, the percentagesof clams in the active, ripe, and partially spentstages were given positive values (multipliedby +1), and the percentages of clams in theinactive and spent stages were given negativevalues (multiplied by -1). These values weresummed for each month at each station, andthese represent the "central tendency of re­production." For example: a month with 30%active, 10% ripe, and 70% inactive clamswould be scored as -30%. A Kruskal-Wallisone-way analysis of variance (ANOVA) wasused to test significance among the monthlycentral tendencies. The coefficient of varia­tion of each month was used to compare thevariation in reproduction between wet anddry years.

To characterize the physical and biologicalenvironment of northern San Francisco Bayduring our study, we used temperature, sa­linity, and chlorophyll data collected by otheragencies. The California Department ofWater Resources (CDWR) collected MallardIsland and Carquinez Strait salinity and tem­perature data every hour using an in situsurface conductivity and temperature sensor(California Department of Water Resources1999). San Pablo Bay data were collectedevery 15 min by the U.S. Geological Survey(USGS) using in situ conductivity and tem­perature sensors on the surface and bottom(Buchanan 1999). These salinity and temper­ature data were summarized to acquire amean monthly value for wet and dry years.Chlorophyll a flux was calculated as describedby Jassby et a1. (1993): multiplication of thecharacteristic surface chlorophyll a concen­tration of the Sacramento and San JoaquinRivers by their outflow rates. These valuesrepresent the estimated carbon from micro­algae that are transported into the bay fromthe freshwater tributaries. Because primaryproduction can be high in these areas, thecarbon fllLx can be substantial (Jassby et a1.1993). Chlorophyll a concentrations for the

334

chlorophyll f l u calculation and for chloro-phyll a concentrations at the MI, CNWS, CS, and SPB sites and for central San Fran-cisco Bay were provided by the USGS (Wienke et al. 1990, 1991, 1992, 1993, Caf-frey et al. 1994, Edmunds et al. 1995, 1997, Baylosis et al. 1997, 1998). Kendall's Tao and Kendall's concordance correlations were used to test significance between reproductive cen-tral tendency and physical parameters.

R E S U L T S

Reproductive Patterns

Potamocorbula amzwensis reached reproductive maturity (i.e., sperm and eggs were present) each year at all four locations. Reproductively active individuals were observed in salinities as low as 0.1 psu (spring, Suisun Bay) and as high as 27.6 psu (summer, San Pablo Bay) and at temperatures ranging from 6.4"C (win-ter, Suisun Bay) to 23.0% (summer, Suisun Bay). There were marked temporal differ-ences in the central tendency of reproduction among the populations of P. amm-ensis.

WET YEARS.During wet years (1993, 1995, 1996, and 1997), a greater percentage of individuals at the stations closer to fresh-water inflow (MI and CNWS) were re-productively active than individuals during dry years (Figure 3). The reproductive central tendency of the MI population (the closest to freshwater inflow) showed reproductive activity for 10 months during wet years. The only months of reproductive inactivity were June and October. The population at the next closest down-bav station. CNWS. was active for 9 months. he populations at ;he stations closer to the marine influence, CS and SPB (Figure 3), were active for shorter periods (8 months) than the populations at the fresher locations.

DRY YEARS. Re~roductive activitv was shorter in duration and a smaller percentage of individuals were reproductive during the dry years (1989-1992, 1994), relative to the wet years, at the stations closest to freshwater inflow (MI, CNWS, and CS) (Figure 3). Al-though there was reproductive activity from January through May at MI, the percentages

PACIFIC SCIENCE . July 2002

of reproductive individuals during dry years show a consistent trend of being lower than u

the percentages during wet years. During the summer and fall, reproductive activity was observed only in September. The MI popu-lation initiated reproductive activity again in November and December. Reproductive activitv in the CNWS ~ o ~ u l a t i o nwas of a

L 1

lesser magnitude and shorter duration dur-ing dry years than during wet years. The CNWS and CS ~o~u la t ionswere active for

L L

4-5 months, primarily from January through April and then again in December at CNWS. SPB animals showed an o ~ ~ o s i t etrend from that seen at the other site; bith reproductive activity greater in duration and in magnitude for most months during the dry years than during wet years (Figure 3). The SPB popula-tion was reproductively active from January to May and again from July through December.

The coefficients of variation for the central tendencies were in phase for dry and wet years during the winter and spring for pop-ulations at the freshest station, during winter and fall at MI and CNWS, although the co-efficient of variation was larger. with one ex-ception, in the dry years i t Lese stations (Figure 4). Peaks in the monthly coefficient of variation at CS were out of ~ h a s efor the wet and dry years only during spring. The co-efficients of variation for the CS population (Figure 4) peaked in summer and fall during the wet years and dry years. Conversely, the coefficient of variation for the CS population was very hlgh in spring of dry years, but the wet-year coefficient of variation was at an annual low during spring. The variability of SPB central tendencv values in wet and drv years was mostly out of phase with the great-est variability occurring during the late spring in the dry years and the late summer in the wet years.

Interannual differences in freshwater inflows from the Sacramento and San Joaquin Rivers are shown by marked differences in salinity distributions in the estuary. Although the daily average salinity dropped between Janu-ary and April during every year of the study,

334

chlorophyll flux calculation and for chloro­phyll a concentrations at the MI, CNWS,CS, and SPB sites and for central San Fran­cisco Bay were provided by the USGS(Wienke et al. 1990, 1991, 1992, 1993, Caf­frey et al. 1994, Edmunds et al. 1995, 1997,Baylosis et a1. 1997, 1998). Kendall's Tao andKendall's concordance correlations were usedto test significance between reproductive cen­tral tendency and physical parameters.

RESULTS

Reproductive Patterns

Potamocorbula amurensis reached reproductivematurity (i.e., sperm and eggs were present)each year at all four locations. Reproductivelyactive individuals were observed in salinitiesas low as 0.1 psu (spring, Suisun Bay) and ashigh as 27.6 psu (summer, San Pablo Bay)and at temperatures ranging from 6.4°C (win­ter, Suisun Bay) to n.o°c (summer, SuisunBay). There were marked temporal differ­ences in the central tendency of reproductionamong the populations of P. amurensis.

WET YEARS. During wet years (1993,1995, 1996, and 1997), a greater percentageof individuals at the stations closer to fresh­water inflow (MI and CNWS) were re­productively active than individuals duringdry years (Figure 3). The reproductive centraltendency of the MI population (the closest tofreshwater inflow) showed reproductiveactivity for 10 months during wet years. Theonly months of reproductive inactivity wereJune and October. The population at the nextclosest down-bay station, CNWS, was activefor 9 months. The populations at the stationscloser to the marine influence, CS and SPB(Figure 3), were active for shorter periods (8months) than the populations at the fresherlocations.

DRY YEARS. Reproductive activity wasshorter in duration and a smaller percentageof individuals were reproductive during thedry years (1989-1992, 1994), relative to thewet years, at the stations closest to freshwaterinflow (MI, CNWS, and CS) (Figure 3). Al­though there was reproductive activity fromJanuary through May at MI, the percentages

PACIFIC SCIENCE· July 2002

of reproductive individuals during dry yearsshow a consistent trend of being lower thanthe percentages during wet years. During thesummer and fall, reproductive activity wasobserved only in September. The MI popu­lation initiated reproductive activity againin November and December. Reproductiveactivity in the CNWS population was of alesser magnitude and shorter duration dur­ing dry years than during wet years. TheCNWS and CS populations were active for4-5 months, primarily from January throughApril and then again in December at CNWS.SPB animals showed an opposite trend fromthat seen at the other sites, with reproductiveactivity greater in duration and in magnitudefor most months during the dry years thanduring wet years (Figure 3). The SPB popula­tion was reproductively active from January toMay and again from July through December.

The coefficients of variation for the centraltendencies were in phase for dry and wetyears during the winter and spring for pop­ulations at the freshest station, during winterand fall at MI and CNWS, although the co­efficient of variation was larger, with one ex­ception, in the dry years at these stations(Figure 4). Peaks in the monthly coefficient ofvariation at CS were out of phase for the wetand dry years only during spring. The co­efficients of variation for the CS population(Figure 4) peaked in summer and fall duringthe wet years and dry years. Conversely, thecoefficient of variation for the CS populationwas very high in spring of dry years, but thewet-year coefficient of variation was at anannual low during spring. The variability ofSPB central tendency values in wet and dryyears was mostly out of phase with the great­est variability occurring during the late springin the dry years and the late summer in thewet years.

DISCUSSION

Interannual differences in freshwater inflowsfrom the Sacramento and San Joaquin Riversare shown by marked differences in salinitydistributions in the estuary. Although thedaily average salinity dropped between Janu­ary and April during every year of the study,

Influence of Hydrologic Processes on Potamocorbula ~murensis . Parchaso and Thompson

. . . , -..

-100 SPB

FIGURE3 . Mean monthly central tendency (percentage with 1 SD) of reproductive (positive) and nonreproductive (negative) populations at the Mallard Island (MI), Concord Naval Weapons Station (CNWS), Carquinez Strait (CS), and San Pablo Bay (SPB) locations during pooled wet (m) and dry (+) years. Central tendency (y axis) is an index that co~llbines the percentage of repoductive individuals (activc, ripe, and spawning, see text for definitions) and non- reproductive inhviduals (inactive and spent). For clarity nonreproductive cenaal tendency values are given negative values. Periods of significant differences between wet and dry years are indicated (',P < 0.10; ", P < 0.05).

corresponding to periods of freshwater in- flows, dry years obviously had substantially higher average salinities than wet years. The salinity at the most up-stream station, Mal- lard Island, and the down-stream station, Carquinez Strait, dropped to 0 psu in the wet years (Figure 5).

S~atial differences in salinitv reflect the estuarine nature of northern San Francisco Bay. Mallard Island, the location farthest up- stream, had the lowest mean monthly salinity values and narrowest range (0 to 10 psu) (Figure 5). In contrast, the mean monthly sa- linity in San Pablo Bay showed a strong ma- rine influence and ranged from 12 to 29 p s ~ . The variability in the mean monthly salinity at the Carquinez Strait station was the great-

est of all the stations sampled, ranging from 2 to 22 psu (Figure 5).

Reproductive individuals of P. amurensis were found throughout the salinity range in- vestigated in this study. However, reproduc- tive seasonality was not consistent among the stations. For example, the Suisun Bay pop- ulations (MI and CNWS) of P. amzwezsis demonstrated a seasonal reproductive cycle that was characterized by a high percentage of reproductive individuals during wet years. In contrast, the San Pablo Bay population, the most marine station, had near-continuous reproductive activity during the high-salinity dry years.

Fluctuations in salinity, particularly in shallow marine areas and estuaries that expe-

Influence of Hydrologic Processes on Potamocorbula amurensis Parchaso and Thompson 335

-60

-80

-100CS

100

80

60

40g 20

.g O+-..,..-.,........,..,V1'""r'..............'b-t+H....r-.~e -20

e -40u -60

-80

-100

MII .'.

100 1 ""I~""""-l.

80

60

40

20S5"0

~] -20

1j -40U

.1, ,

100 I ................e.-.­

80

60

~ 40>,

5 20"0~ O+-..,..-.........,..,...,..IjtT'fT-~IItrT-rttr9-T--.

] -20

~ -40

-60

-80

-100CNWS

100"1 .._..........:80111]1",.....t'&.

60t!:->, 40

:c5 20~ o+-.,...........~~..,..Pt-+-r-h-~-Hr ......-,- -20 an.fjc -40"u -60

-80

-100SPB

FIGURE 3. Mean monthly central tendency (percentage with 1 SD) of reproductive (positive) and nonreproductive(negative) populations at the Mallard Island (MI), Concord Naval Weapons Station (CNWS), Carquinez Strait (CS),and San Pablo Bay (SPB) locations during pooled wet (.) and dry (.) years. Central tendency (y axis) is an index thatcombines the percentage of reproductive individuals (active, ripe, and spawning, see text for definitions) and non­reproductive individuals (inactive and spent). For clarity nonreproductive central tendency values are given negativevalues. Periods of significant differences between wet and dry years are indicated (*, P < 0.10; **, P < 0.05).

corresponding to periods of freshwater in­flows, dry years obviously had substantiallyhigher average salinities than wet years. Thesalinity at the most up-stream station, Mal­lard Island, and the down-stream station,Carquinez Strait, dropped to 0 psu in the wetyears (Figure 5).

Spatial differences in salinity reflect theestuarine nature of northern San FranciscoBay. Mallard Island, the location farthest up­stream, had the lowest mean monthly salinityvalues and narrowest range (0 to 10 psu)(Figure 5). In contrast, the mean monthly sa­linity in San Pablo Bay showed a strong ma­rine influence and ranged from 12 to 29 psu.The variability in the mean monthly salinityat the Carquinez Strait station was the great-

est of all the stations sampled, ranging from 2to 22 psu (Figure 5).

Reproductive individuals of P. amw"ensiswere found throughout the salinity range in­vestigated in this study. However, reproduc­tive seasonality was not consistent among thestations. For example, the Suisun Bay pop­ulations (MI and CNWS) of P. amurensisdemonstrated a seasonal reproductive cyclethat was characterized by a high percentageof reproductive individuals during wet years.In contrast, the San Pablo Bay population,the most marine station, had near-continuousreproductive activity during the high-salinitydry years.

Fluctuations in salinity, particularly inshallow marine areas and estuaries that expe-

PACIFIC SCIENCE . July 2002

Jan Mar May Jul Sep Nov Jan Mar May Jul Sep Nov

MI CS

Jan Mar May Jul Sep Nov Jan Mar May Jul Sep Nov

CNWS SPB

FIGURE4. Variability of central tendency of individuals at the Mallard Island (MI), Concord Naval Weapons Station (CNWS), Carquinez Strait (CS), and San Pablo Bay (SPB) locations during pooled wet (m) and dry (4)years.

rience large and prolonged changes in salinity during periods of heavy rainfall, have been suggested as possible factors for regulating reproduction in some marine invertebrates (Giese and Pearse 1974, 1979). For example, Wilson (1969) showed that gametogenesis and spawning in a Western Australian estua- rine mussel, Xenostrobus secum, are related to salinity fluctuations, and that spawning occurs at different times in several populations, in each case correlated with a critical salinity level. The onset of gametogenesis, matura- tion of gametes, and spawning occurs in syn- chrony with periods of rainfall each year, regardless of the timing of the rainfall periods and thus regardless of temperature within a given year. We show here that the processes that determine patterns of salinity (i.e., fresh- water flow) also appear to control the repro- ductive patterns of P. anzurensis in northern San Francisco Bay, but that neither salinity nor temperature are, by themselves, control- ling factors of reproduction.

The recorded average mean monthly tem- perature at all locations showed seasonal variability (Figure 5) and little interannual variation. There was little spatial variability in the mean monthly values. Throughout the sample locations, the mean monthly temper- atures ranged from 8 to 22°C. Reproduc­tive activity at all the stations was observed throughout the observed temperature range (Figure 6).

The differences in reproductive patterns between wet and dry years in Suisun Bay are associated with variations in freshwater flow into Suisun Bay from the Sacramento and San Joaquin Rivers, but are not specifically related to some critical salinity, temperature, or volume of freshwater flow. We suggest that the seasonality of reproduction in Suisun Bay populations is linked to the seasonal na- ture of locally produced phytoplankton and river-borne food supplies. Because of its abil- ity to efficiently filter and assimilate a wide range of particle sizes and food types, from

336 PACIFIC SCIENCE· July 2002

2 ~ 2

" I "0 0

:~ 1.5I

.~1.5'1:;;;; "> >

'-I 1 '-

0 0

E "" "u

0.51u

IE i:E 0.5" "0

I0

u u0 0

Jan Mar May Jul Sep Nov Jan Mar May Jul Sep Nov

MI CS

2 2 l" "0 .S J.~

1.5 tii'1:; '1:; 1.5

1" "> >'- '-

I ~0 0

E ;::I" "u u

IE 0.5<;:::

0.51'-" "c c

U U

0 0

Jan Mar May Jul Sep Nov Jan Mar May Jut Sep Nov

CNWS SPB

FIGURE 4. Variability of central tendency of individuals at the Mallard Island (MI), Concord Naval Weapons Station(CNWS), Carquinez Strait (CS), and San Pablo Bay (SPB) locations during pooled wet (_) and dry (.) years.

rience large and prolonged changes in salinityduring periods of heavy rainfall, have beensuggested as possible factors for regulatingreproduction in some marine invertebrates(Giese and Pearse 1974, 1979). For example,Wilson (1969) showed that gametogenesisand spawning in a Western Australian estua­rine mussel, Xenostrobus securus, are related tosalinity fluctuations, and that spawning occursat different times in several populations, ineach case correlated with a critical salinitylevel. The onset of gametogenesis, matura­tion of gametes, and spawning occurs in syn­chrony with periods of rainfall each year,regardless of the timing of the rainfall periodsand thus regardless of temperature within agiven year. We show here that the processesthat determine patterns of salinity (i.e., fresh­water flow) also appear to control the repro­ductive patterns of P. anzurensis in northernSan Francisco Bay, but that neither salinitynor temperature are, by themselves, control­ling factors of reproduction.

The recorded average mean monthly tem­perature at all locations showed seasonalvariability (Figure 5) and little interannualvariation. There was little spatial variability inthe mean monthly values. Throughout thesample locations, the mean monthly temper­atures ranged from 8 to 22°C. Reproduc­tive activity at all the stations was observedthroughout the observed temperature range(Figure 6).

The differences in reproductive patternsbetween wet and dry years in Suisun Bay areassociated with variations in freshwater flowinto Suisun Bay from the Sacramento andSan Joaquin Rivers, but are not specificallyrelated to some critical salinity, temperature,or volume of freshwater flow. We suggestthat the seasonality of reproduction in SuisunBay populations is linked to the seasonal na­ture of locally produced phytoplankton andriver-borne food supplies. Because of its abil­ity to efficiently filter ami assimilate a widerange of particle sizes and food types, from

Jan Mar May Jul Sep Nov

Salinity MI

Jan Mar May Jul Sep Nov

Salinity CS

-Jan Mar May Jul Sep Nov

Salinity SPB

O L - , , , , Jan Mar May Jul Sep Nov

Temperature for all stations

FIGURE5. Mean monthly salinity (psu) at the Mallard Island (MI), Carquinez Strait (CS), and San Pablo Bay (SPB) locations during pooled wet (W) and dry (+) years; mean monthly temperature ( C + 1 SD) at the Mallard Island, Carquinez Stnit, and San Pablo Bay locations during pooled wet (W) and dry (+) years.

14

12

~10

C 8.0:8 6-;;;

4VJ

2

0

Jan Mar May Jul Sep Nov

Salinity MI

30

25

~ 20C.0 15:5-;;; \0VJ

5

0

Jan Mar May Jul Sep Nov

Salinity CS

35

30

S 25·

820.0:5 15-;;;

10VJ

5

0

Jan Mar May Jul Sep Nov

Salinity SPB

25i

~ 20 1

il5~~g, /0

~ : ..~Jan Mar ~ay Jul Sep Nov

Temperature for all stations

FIGURE 5. Mean monthly salinity (psu) at the Mallard Island (MI), Carquinez Strait (CS), and San Pablo Bay (SPB)locations during pooled wet (.) and dry (.) years; mean monthly temperature ("C ± 1 SD) at the Mallard Island,Carquinez Strait, and San Pablo Bay locations during pooled wet (.) and dry (.) years.

PACIFIC SCIENCE . July 2002

. ++.. M

Mean Temperature Mean Temperature

MI Dry year Mi Wet year

-100 J y.

Mean Temperature Mean Temperature

C-S Dry year CS Wet year

Mean Temperature Mean Temperature

SPB Dry year SPB Wet year

FIGURE 6. Scatter plot of temperature versus central tendency (see text) at the Mallard Island (MI), Carquinez Strait (CS), and San Pablo Bay (SPB) locations during pooled wet and dry years.

phytoplankton to free and particle-bound bac- seasonal patterns of freshwater flow are di- teria (Decho and Luoma 1991, Werner and rectly related to the quantity and quality of Hollibaugh 1993), P. amurensis is able to use a carbon in this system. Up to 75% of the car- variety of food resources. We know that the bon found in Suisun Bay could be traced to

338 PACIFIC SCIENCE· July 2002

Mean TemperatureL-. .._

Mean Temperature

I~-~------~----~--Ir-~----~--~-----l

I 100 j .. ...... I 100 l ....1''''.... I•• • Ii.. I

i$' 50 , • I g 50i·.. . II

~. I ~ l ··~ 0 -l--. • I ~ 0 +---,----r---___,~-___,] 5to 10.00 15.00 '0.00· 25.00 I ] 5. 0 10.00 15.00 •.~O 25.00'" I '" I .vU -50 •• • U -50 1

•• I I-100 .. I -100 j •

III

MI Dry year Mi Wet year

25.00

..Mean Temperature

............ ..100 1

I50 1

Io +-1-----,---...~__4.~.~,--5bo 10.00 15.00 20.0tt

-501 ••

-100 J

liI) ;>,

I I ~I I '"

II ~

25.00 ! I "'§U~I I

I I

I

IMean Temperature

100 l :.~:. ••i$' 501· •••

] 0 t';----:- ... ..~ 5. 0 10.00 .15.00 20.00

U -50 • • ••

•••-100 ...

CS Wet year

.......• •.. .GS Dry year

100 1 ~ - ••••;>, 50 j • .:. •

~ l-~~ .....,~ ..~ 0 •] 5. 0 10.00 .,.00. '0.00

~ -50 ji • •

-100 •

10.00

•. ., .

1500 .'0.00...•

25.00

Mean Temperature Mean Temperature

SPB Dry year SPB Wet year

FIGURE 6. Scatter plot of temperature versus central tendency (see text) at the Mallard Island (MI), Carquinez Strait(CS), and San Pablo Bay (SPB) locations during pooled wet and dry years.

phytoplankton to free and particle-bound bac­teria (Decho and Luoma 1991, Werner andHollibaugh 1993), P. amurensis is able to use avariety of food resources. \Ve know that the

seasonal patterns of freshwater flow are di­rectly related to the quantity and quality ofcarbon in this system. Up to 75% of the car­bon found in Suisun Bay could be traced to

--

- - - - -

339Influence of Hydrologic Processes on Pota7nocorbuh amuremis . Pa~chasoand Thompson

riverine inputs (Jassby et al. 1993) before the elimination of the phytoplankton bloom in 1987. With the introduction of P. amurensis to the system, allochthonous sources of car-bon are likely to be even more important than autochthonous sources of carbon (Scheme1 et al. 1996). We also know that the timing of freshwater inputs is critical to the quality of food available to organisms in Suisun Bay. Although freshwater transports suspended solids from the Sacramento and San Joaquin Rivers into Suisun Bay, the relationship be-tween freshwater outflow and suspended solid concentration and the concentration of labile carbon is not correlated. The initial pulse of freshwater from the first rains of the rainy season, usually in the late fall or early winter, is the greatest source of suspended solids into Suisun Bay (Ruhl and Shoelhammer 1997) and is likely to be a combination of near-field watershed and marsh sediments and particu-late matter (Jassby and Cloern 2000). Subse-quent rain and snowrnelt events transport suspended solids downstream but not at the same magnitude or with the same high per-centage of labile carbon (Canuel and Cloern 1996) as the first pulse of the rainy season.

Food transported into Suisun by way of this first freshwater pulse may be the energy source that initiates reproductive activity in P. amurensis in winter. This is the most consis-tent reproductive cue seen for P. anrurensis

during all wet years as shown by the low variability in positive reproductive activity during this ~ e r i o dke..

2 the coefficient of u ..

variation of the reproductive central tendency was consistently low during wet winters) (Figure 4). The lack of large storms during dry years produces less particulate carbon (Jassby and Cloern 2000) and is less likely to produce a large, one-time pulse of particulate carbon from the spatially disparate sources of carbon, the distant watershed and nearby marshes. As we might exDect. this cue was less

U L ,

temporally consistent during the dry years and the coefficients of variation during winter were thus larger in dm vears than in wet

U i d

years. Because this cue for initiation of re-production is not linearly related to fresh-water flow (i.e., maximum reproductive activ-ity does not occur at minimum or maximum freshwater flow volumes), we would not ex-pect, nor do we see, a strong correlation be-tween these variables (Table 1).

It is likely that some riverine sources of food are supplied to P. amurensis throughout the year. I t is unknown what percentage of the suspended solids that are transported into the bav contain bioavailable carbon at the

i

time of transport and how much is trans-formed in transit. It is clear that there are bacteria living on these particles once they enter the bay and that they are both produc-tive (Hollibaugh and Wong 1996) and sea-

TABLE l

Significant Kendall's Tao and Kendall's Concordance Values for Central Tendency Versus Chlorophyll a Concentration, Chlorophyll a F l u , and Freshwater Flow for Pooled Wet and Dry Years

Station Water Year Factor Kendall Tao Factor Kendall Concordance

MI

CNWS

Dry Wet Dry Wet

-Freshwater flow -

Chlorophyll a

0.30*

0.46*"

Chlorophyll a and chlorophyll flux Chlorophyll a and chlorophyll flux Chlorophyll a and chlorophyll flux Chlorophyll a and chlorophyll f l u

0.87*" 0.77*'* 0.75"' 0.76""

CS Dry Chlorophyll flux -

0.41"' Chlorophyll a and chlorophyll flux 0.75"

SPB

Wet

DV

Chlorophyll a Chlorophyll flux -

0.50*" 0.28'

-

Chlorophyll a and chlorophyll flux 0.87'* Wet Chlorophyll flux 0.37*" Chlorophyll a and chlorophyll flux 0.80"'

Note: Significantly related physical factors were not included in these analyses.', P < 0.05; **, P < 0.01; "*, P < 0.001.

Influence of Hydrologic Processes on Potamocorbula amurensis . Pa1'chaso and Thompson 339

riverine inputs (Jassby et aI. 1993) before theelimination of the phytoplankton bloom in1987. With the introduction of P. amurensisto the system, allochthonous sources of car­bon are likely to be even more important thanautochthonous sources of carbon (Schemel etal. 1996). We also know that the timing offreshwater inputs is critical to the quality offood available to organisms in Suisun Bay.Although freshwater transports suspendedsolids from the Sacramento and San JoaquinRivers into Suisun Bay, the relationship be­tween freshwater outflow and suspended solidconcentration and the concentration of labilecarbon is not correlated. The initial pulse offreshwater from the first rains of the rainyseason, usually in the late fall or early winter,is the greatest source of suspended solids intoSuisun Bay (Ruhl and Shoelhammer 1997)and is likely to be a combination of near-fieldwatershed and marsh sediments and particu­late matter (Jassby and Cloern 2000). Subse­quent rain and snowmelt events transportsuspended solids downstream but not at thesame magnitude or with the same high per­centage of labile carbon (Canuel and Cloern1996) as the first pulse of the rainy season.

Food transported into Suisun by way ofthis first freshwater pulse may be the energysource that initiates reproductive activity in P.amurensis in winter. This is the most consis­tent reproductive cue seen for P. amurensis

during all wet years as shown by the lowvariability in positive reproductive activityduring this period (i.e., the coefficient ofvariation of the reproductive central tendencywas consistently low during wet winters)(Figure 4). The lack of large storms duringdry years produces less particulate carbon(Jassby and Cloern 2000) and is less likely toproduce a large, one-time pulse of particulatecarbon from the spatially disparate sourcesof carbon, the distant watershed and nearbymarshes. As we might expect, this cue was lesstemporally consistent during the dry yearsand the coefficients of variation during winterwere thus larger in dry years than in wetyears. Because this cue for initiation of re­production is not linearly related to fresh­water flow (i.e., maximum reproductive activ­ity does not occur at minimum or maximumfreshwater flow volumes), we would not ex­pect, nor do we see, a strong correlation be­tween these variables (Table 1).

It is likely that some riverine sources offood are supplied to P. amurensis throughoutthe year. It is unknown what percentage ofthe suspended solids that are transported intothe bay contain bioavailable carbon at thetime of transport and how much is trans­formed in transit. It is clear that there arebacteria living on these particles once theyenter the bay and that they are both produc­tive (Hollibaugh and Wong 1996) and sea-

TABLE 1

Significant Kendall's Tao and Kendall's Concordance Values for Central Tendency Versus Chlorophyll aConcentration, Chlorophyll a Flux, and Freshwater Flow for Pooled Wet and Dry Years

Station \Vater Year Factor Kendall Tao Factor Kendall Concordance

MI Dry Chlorophyll a and chlorophyll flux 0.87***\Vet Freshwater flow 0.30* Chlorophyll a and chlorophyll flux 0.77***

CNWS Dry Chlorophyll a and chlorophyll flux 0.75***\Vet Chlorophyll a 0.46*** Chlorophyll a and chlorophyll flux 0.76***

Chlorophyll flux 0.41 ***CS Dry Chlorophyll a and chlorophyll flux 0.75**

\Vet Chlorophyll a 0.50***Chlorophyll flux 0.28*

SPB Dry Chlorophyll a and chlorophyll flux 0.87**Wet Chlorophyll flux 0.37*** Chlorophyll a and chlorophyll flux 0.80***

Note: Significandy related physical faerors were not included in these analyses.*, P < 0.05; **, P < 0.01; ***, P < 0.001.

PACIFIC SCIENCE . July ZOO2

FIGURE7. Chlorophyll R flux into Suisun Bay from the Sacramento-San Joaquin Rwer Delta from 1986 to 1998.

sonally varying (Murrel et al. 1999). The abundance of article-associated bacteria re-

I

mains constant between April and July, and declines in August during which time the abundance of free-living bacteria concurrently increases (Murrel et al. 1999). Because P. amurensis is capable of feeding on free-living bacteria (Werner and Hollibaugh 1993), it is likelv that riverine sources of caFbon through- " out the year are providing, at the least, a source of bacterial food, if not particulate food. The consum~tion of thls food source bv P. amureasis may contribute to the summer decline in particle-associated bacteria (Murrel et al. 1999).

~ocal1~'~roducedphytoplankton and phy- toplankton transported from other regions in the svstem are likelv to be additional sources of fobd for P. amuiensis. Phytoplankton pro- duction in the bay and in the rivers is highest in the spring through late summer due to seasonal increases in hydraulic residence times and irradiance. Although phytoplankton bio- mass has declined in the northern bay since 1987, the higher primary production during these seasons is likely to increase the impor- tance of phytoplankton as a food supply to P.

amurerzsis during spring and summer. The ~ositive rank correlation between central ten- I

dency and chlorophyll a concentration at two of the four sites (Table 1) supports this hy- pothesis. Phytoplankton from the tributaries also enters the bav as bioavailable carbon when phytoplanktoA growth rate exceeds res- piration and consumption in the Sacramento- San Joaquin Delta. Freshwater phytoplankton is transported into Suisun Bay throughout the year, but a peak in this transported carbon (shown as chlorophyll a flux, Figure 7) occurs when peak flows and high chlorophyll a con­centrations are coincident. The amount of chloro~hvlla trans~orted into Suisun Bav

I i

during wet years was substantially greater than during dry years.

We suggest that food in~u t s from later UU

freshwater pulses are the cue that determines the length of reproductive activity in spring. During wet years, freshwater input is pro- tracted and food sources such as riverine phytoplankton become available to even the most down-bay populations. The magnitude of chlorophyll a flux into Suisun Bay from the delta varied little in magnitude during dry years (1 989-1 992 and 1994), but consistently

340

8.E+IO

7.E+10

6.E+10

';j) 5.E+1OOIl5'" 4.E+1O:::l

i:2>,~ 3.E+10Q,

e0:;::

2.E+10u

I.E+ 10

O.E+OO

PACIFIC SCIENCE· July 2002

..

-I.E+IO .----.----,----.---. --,------,------.--. ----,------,

1986 1988 1990 1992 1994 1996 1998

FIGURE 7. Chlorophyll a flux into Suisun Bay from the Sacramento-San Joaquin River Delta from 1986 to 1998.

sonally varying (Murrel et al. 1999). Theabundance of particle-associated bacteria re­mains constant between April and July, anddeclines in August during which time theabundance of free-living bacteria concurrentlyincreases (Murre! et al. 1999). Because P.amurensis is capable of feeding on free-livingbacteria (Werner and Hollibaugh 1993), it islikely that riverine sources of carbon through­out the year are providing, at the least, asource of bacterial food, if not particulatefood. The consumption of this food source byp. amurensis may contribute to the summerdecline in particle-associated bacteria (Murrelet al. 1999).

Locally produced phytoplankton and phy­toplankton transported from other regions inthe system are likely to be additional sourcesof food for P. amurensis. Phytoplankton pro­duction in the bay and in the rivers is highestin the spring through late summer due toseasonal increases in hydraulic residence timesand irradiance. Although phytoplankton bio­mass has declined in the northern bay since1987, the higher primary production duringthese seasons is likely to increase the impor­tance of phytoplankton as a food supply to P.

amurensis during spring and summer. Thepositive rank correlation between central ten­dency and chlorophyll a concentration at twoof the four sites (Table 1) supports this hy­pothesis. Phytoplankton from the tributariesalso enters the bay as bioavailable carbonwhen phytoplankton growth rate exceeds res­piration and consumption in the Sacramento­San Joaquin Delta. Freshwater phytoplanktonis transported into Suisun Bay throughout theyear, but a peak in this transported carbon(shown as chlorophyll a flux, Figure 7) occurswhen peak flows and high chlorophyll a con­centrations are coincident. The amount ofchlorophyll a transported into Suisun Bayduring wet years was substantially greaterthan during dry years.

We suggest that food inputs from laterfreshwater pulses are the cue that determinesthe length of reproductive activity in spring.During wet years, freshwater input is pro­tracted and food sources such as riverinephytoplankton become available to even themost down-bay populations. The magnirudeof chlorophyll a flux into Suisun Bay from thedelta varied little in magnirude during dryyears (1989-1992 and 1994), but consistently

341Influence of Hydrologic Processes on Potamocorbula a~nurensis. Parchaso mid Thompson

peaked during the spring. Chlorophyll a flux during the wet years also peaked during the spring, but at a greater magnitude and for a longer period than in dry years (Figure 7). This higher chlorophyll a flux during wet-year springs may be responsible for the pro-tracted reproductive activity during wet years. Reproductive periods were 3 months longer during wet years than during the dry years and were significantlyrelated to chlorophyll a flux at the midgradient stations (CNWS and CS). Chlorophyll a flux was low during dry years (Figure 7), and this food source may have been de~letedand diluted as it was transported ddwn the bay. Consistent with this pattern, clams at the station closest to the freshwater source and closest to the transDort of riverine phytoplankton (MI) have a longer reproductive period during dry years than the down-bay populations (Figure 4).

The temporal pattern in the coefficients of variation supports these hypotheses. The low coefficient of variation (i.e., synchronous re-productive activity) during wet springs is due to a strong seasonal cycle in chlorophyll a flux. The timing of the chlorophyll a flux ~ e a kis controlled bv a combination of the timing of sufficient river outflow to transport the river-borne phytoplankton into the bay and the seasonal increase in phytoplankton growth rate. The peak chlorophyll a flux is thus a function of the seasonally consistent irradiance cycle; spring river outflow is mostly a result of snowmelt that occurs in May and June (Cayan et al. 1997), and phytoplankton growth rate is primarily controlled by light availabilitv in this svstem (Lehman 1996). Thus, it is not the period of maximum out-flow or maximum chlorophyll a concentra-tion that controls the ~ e a kchloro~hvlla flux.

1 i

but the period whei their product which is most related to irradiance. As we might expect, the pattern of freshwater flow during dry springs, with varying amounts of low snow accumulation and varying levels of irradiance needed to melt the snow, is less consistent between vears because snowmelt maxima are a function of both snow accumu-lation and irradiance (Cayan et al. 1997). Thus. interannual variabilitv in the snowmelt runoff during dry years leads to more vari-

ability in this food signal and thus in more seasonally variable reproductive activity dur-ing the dry years; note that chlorophyll a flux was never significantly related to P. amurensis reproduction in dry years (Table 1). This increased variability in reproductive activity is true even at the freshest station. which is most likely to benefit from this food source during low runoff years.

It would be hel~fulto examine the rela-tionship of the combination of these physical factors with central tendency to establish their additive effects. However, the established im-portant physical factors, local chlorophyll a , chlorophyll a flux, and freshwater inflow, are frequently related to each other (i.e., fresh-water flow is commonlv related to chloro-phyll a flux, particularly in dry years, and local chlorophyll a concentrations can include chlorophyll a that is being delivered from the rivers if the freshwater ~hvto~lanktonare still

L , L

viable). Given these constraints we were able to test the significance of the relationship of local chlorophyll a concentration, chlorophyll a flux, and central tendency during all but one period (Table 1). In all cases tested, there was a significant relationship (Kendall's concor-dance ranges from 0.75 to 0.87), and the sig-nificance of the combined physical factors was similar to, or greater than, that seen with simple rank correLtions.

We hypothesize that the San Pablo Bay populations showed distinctly different re-productive patterns than ~uisunBay pop-ulations due to the different sources of food used by these populations. San Pablo Bay ~ o ~ u l a t i o n smav receive food from a combi-1 I

nation of freshwater, marine (central bay), and locally derived sources. During dry years, phytoplankton biomass and primary produc-tion in San Pablo Bay is usually greater than in Suisun Bay (Alpine and Cloern 1992), which was the case in this study for all but 1 y r (Figure 8). In addition, local chlorophyll a concentrations are more likely to be aug-mented by oceanic phytoplankton during the spring and summer due to larger tidal ex-cursions into San Pablo Bay during low run-off periods. Chlorophyll a concentrations in central San Francisco Bav (Fieure 8). the

2 , " ,,

most marine region of San Francisco Bay,

Influence of Hydrologic Processes on Potamocorbula amurensis . Parchaso and Thompson 341

peaked during the spring. Chlorophyll a fluxduring the wet years also peaked during thespring, but at a greater magnitude and for alonger period than in dry years (Figure 7).This higher chlorophyll a flux during wet­year springs may be responsible for the pro­tracted reproductive activity during wet years.Reproductive periods were 3 months longerduring wet years than during the dry yearsand were significantly related to chlorophyll aflux at the midgradient stations (CNWS andCS). Chlorophyll a flux was low during dryyears (Figure 7), and this food source mayhave been depleted and diluted as it wastransported down the bay. Consistent withthis pattern, clams at the station closest to thefreshwater source and closest to the transportof riverine phytoplankton (MI) have a longerreproductive period during dry years than thedown-bay populations (Figure 4).

The temporal pattern in the coefficients ofvariation supports these hypotheses. The lowcoefficient of variation (i.e., synchronous re­productive activity) during wet springs is dueto a strong seasonal cycle in chlorophyll aflux. The timing of the chlorophyll a fluxpeak is controlled by a combination of thetiming of sufficient river outflow to transportthe river-borne phytoplankton into the bayand the seasonal increase in phytoplanktongrowth rate. The peak chlorophyll a flux isthus a function of the seasonally consistentirradiance cycle; spring river outflow is mostlya result of snowmelt that occurs in May andJune (Cayan et a1. 1997), and phytoplanktongrowth rate is primarily controlled by lightavailability in this system (Lehman 1996).Thus, it is not the period of maximum out­flow or maximum chlorophyll a concentra­tion that controls the peak chlorophyll a flux,but the period when their product peaks,which is most related to irradiance. As wemight expect, the pattern of freshwater flowduring dry springs, with varying amounts oflow snow accumulation and varying levels ofirradiance needed to melt the snow, is lessconsistent between years because snowmeltmaxima are a function of both snow accumu­lation and irradiance (Cayan et a1. 1997).Thus, interannual variability in the snowmeltrunoff during dry years leads to more vari-

ability in this food signal and thus in moreseasonally variable reproductive activity dur­ing the dry years; note that chlorophyll a fluxwas never significantly related to P. amurensisreproduction in dry years (Table 1). Thisincreased variability in reproductive activityis true even at the freshest station, which ismost likely to benefit from this food sourceduring low runoff years.

It would be helpful to examine the rela­tionship of the combination of these physicalfactors with central tendency to establish theiradditive effects. However, the established im­portant physical factors, local chlorophyll a,chlorophyll a flux, and freshwater inflow, arefrequently related to each other (i.e., fresh­water flow is commonly related to chloro­phyll a flux, particularly in dry years, andlocal chlorophyll a concentrations can includechlorophyll a that is being delivered from therivers if the freshwater phytoplankton are stillviable). Given these constraints we were ableto test the significance of the relationship oflocal chlorophyll a concentration, chlorophylla flux, and central tendency during all but oneperiod (Table 1). In all cases tested, there wasa significant relationship (Kendall's concor­dance ranges from 0.75 to 0.87), and the sig­nificance of the combined physical factorswas similar to, or greater than, that seen withsimple rank correlations.

We hypothesize that the San Pablo Baypopulations showed distinctly different re­productive patterns than Suisun Bay pop­ulations due to the different sources of foodused by these populations. San Pablo Baypopulations may receive food from a combi­nation of freshwater, marine (central bay),and locally derived sources. During dry years,phytoplankton biomass and primary produc­tion in San Pablo Bay is usually greater thanin Suisun Bay (Alpine and Cloern 1992),which was the case in this study for all but1 yr (Figure 8). In addition, local chlorophylla concentrations are more likely to be aug­mented by oceanic phytoplankton during thespring and summer due to larger tidal ex­cursions into San Pablo Bay during low run­off periods. Chlorophyll a concentrations incentral San Francisco Bay (Figure 8), themost marIne region of San Francisco Bay,

PACIFIC SCIENCE . July 2002

F I G U R E . .8. Calculated chloro~hvll iz concentrations at MI (+), C N W S (-), CS (A) , SPB (O), and central San Fran cisco Bay (W).

from which high-salinity water can be tidally advected into San Pablo Bay, can peak in both spring and summer, but they show no hydrologically consistent pattern, because high values occur during dry and wet years. Thus, it is a combination of river-transported carbon, locally derived phytoplankton (which peaks in spring and fall in wet years, Figure 8), and marine phytoplankton (which peaks in spring and summer) that provides the near- continuous food source for this population (Figure 8). These multiple sources are appar- ently sufficient to support near-continuous reproduction (10 months of the year) during dry years (Figure 3).

Although there are large differences in the reproductive patterns of Suisun Bay and San Pablo Bay populations of P. amurensis, there is no evidence that the differences can be at- tributed to genetic differences. The bay pop- ulation as a whole maintains high levels of genetic diversity, as measured in degrees of heterozygosity, levels of polymorphism, and the number of alleles per locus, but no dis- tinct genetic difference was found between

the populations sampled (Duda 1992). A high degree of genetic variability, allowing an organism to have flexibility to respond to changes in environmental factors, could be a factor in the variable re~roductive s t ra te~es u

and, thus, the success of P. amurensis in colo- nizing and establishing itself in San Francisco B av.

One of our motivating factors in doing this study was to examine the reproductive char- acteristics of P. amurensis that might contrib- ute to its success as an invading s~icies . In the

u L

estuarine environment, some of the factors that invading species must adapt to include seasonal variations in salinitv. temDerature. ,, food supply, and predators. Presuming an invading species requires an opening in the community or a high number of propagules (Levine 2000), this opening can be used if individuals of a species have a greater toler- ance to environmental extremes. the abilitv to outcompete an existing species in the utiliza- tion of a resource, and are capable of pro- ducing a large number of larvae under a wider variety of conditions. It has been shown that

342 PACIFIC SCIENCE· July 2002

9.00

8.00

7.00

~5 6.00

";;,-a 5.008oe 4.00

"C

"<i

] 3.00

U2.00

1.00

0.00

1989 1990 1991 1992 1993 1994 1995 1996 1997

FIGURE 8. Calculated chlorophyll 11 concentrations at MI (.), CN\VS (-), CS (.), SPB (e), and central San Fran­cisco Bay (.).

from which high-salinity water can be tidallyadvected into San Pablo Bay, can peak inboth spring and summer, but they showno hydrologically consistent pattern, becausehigh values occur during dry and wet years.Thus, it is a combination of river-transportedcarbon, locally derived phytoplankton (whichpeaks in spring and fall in wet years, Figure8), and marine phytoplankton (which peaks inspring and summer) that provides the near­continuous food source for this population(Figure 8). These multiple sources are appar­ently sufficient to support near-continuousreproduction (10 months of the year) duringdry years (Figure 3).

Although there are large differences in thereproductive patterns of Suisun Bay and SanPablo Bay populations of P. amurensis, thereis no evidence that the differences can be at­tributed to genetic differences. The bay pop­ulation as a whole maintains high levels ofgenetic diversity, as measured in degrees ofheterozygosity, levels of polymorphism, andthe number of alleles per locus, but no dis­tinct genetic difference was found between

the populations sampled (Duda 1992). A highdegree of genetic variability, allowing anorganism to have flexibility to respond tochanges in environmental factors, could be afactor in the variable reproductive strategiesand, thus, the success of P. amurensis in colo­nizing and establishing itself in San FranciscoBay.

One of our motivating factors in doing thisstudy was to examine the reproductive char­acteristics of P. amurensis that might contrib­ute to its success as an invading species. In theestuarine environment, some of the factorsthat invading species must adapt to includeseasonal variations in salinity, temperature,food supply, and predators. Presuming aninvading species requires an opening in thecommunity or a high number of propagules(Levine 2000), this opening can be used ifindividuals of a species have a greater toler­ance to environmental extremes, the ability tooutcompete an existing species in the utiliza­tion of a resource, and are capable of pro­ducing a large number of larvae under a widervariety of conditions. It has been shown that

Influence of Hydrologic Processes on Potamocorhda amurensir . Parchaso and Thompson 343

P. amurensis larvae are capable of surviving a large range in salinity and temperature ( ~ i - colini and Penry 2000). Thus, it is likely that once P. amurensis settled into San Francisco Bay, its ability to (1) utilize locally available, but varylng sources of food resources to maximize reproductive activity, (2) withstand and reproduce during wide changes in salinity and temperature, and (3) survive as a larva in a wide range of salinities and temperatures allowed P. amurensis to ~roduce manv larvae and establish a continuing presence in the benthic community of San Francisco Bay.

ACKNOWLEDGMENTS

We gratefully acknowledge Cindy Brown, Thomas Duda, Oscar Mace, Scott Shapley, and Michelle Shouse for their assistance in the field; Byron Richards and Scott Conard of the R/V Polaris; and Dave Menaugh and his crew for their histology work. We thank Sam Luoma, Fred Nichols, and two anonymous reviewers for reviewing this work.

Literature Cited

Alpine, A. E., and J. E. Cloern. 1992. Trophic interactions and direct physical effects control phytoplankton biomass and pro- duction in an estuary. Limnol. Oceanogr. 37:946-955.

Baylosis, J. I., J. L. Edmunds, B. E. Cole, and J. E. Cloern. 1997. Studies of the San Francisco Bay, California estuarine eco- system: Pilot regional monitoring results, 1996. U.S. Geological Survey Open-File Report 97-598.

Baylosis, J. I., B. E. Cole, and J. E. Cloern. 1998. Studies of the San Francisco Bay, California estuarine ecosystem: Regional monitoring results, 1997. U.S. Geological Survey Open-File Report 98-168.

Buchanan, P. A. 1999. Specific conductance, water temperature and water level data, San Francisco Bay, California, water year 1998. IEP (Interagency Ecol. Program) Newsl. 14 (4): 46.

Caffrey, J. M., B. E. Cole, J. E. Cloern, J. R. Rudek, A. C. Tyler, and A. D. Jassby. 1994. Studies of the plankton and its envi-

ronment in the San Francisco Bay Estuary, California: Regional monitoring results, 1993. U.S. Geological Survey Open-File Report 94-82.

California Department of Water Resources. 1999. California data exchange center (http://cdec.water.ca.gov/).

Canuel, E. A., and J. E. Cloern. 1996. Re- gional differences in the origins of organic matter in the San Francisco Bay ecosys- tem. Pages 305-324 in J. T. Hollibaugh, ed. San Francisco Bay: The ecosystem. American Association for the Advance- ment of Science, Pacific Division, San Francisco.

Carlton, J. T., J. K. Thompson, L. E. Sche- mel, and F. H. Nichols. 1990. Remarkable invasion of San Francisco Bay (California, USA) by the Asian clam Potamocorbula amurensis. I. Introduction and dispersal. Mar. Ecol. Prog. Ser. 66:81-94.

Cayan, D. R., D. H. Peterson, L. fiddle, M. D. Dettinger, and R. Smith. 1997. Spring runoff pulse from the Sierra Nevada. IEP (Interagency Ecol. Program) Newsl. 10 (3): 25-28.

Cloern, J. E. 1982. Does the benthos control phytoplankton biomass in South San Fran- cisco Bay? Mar. Ecol. Prog. Ser. 9:191- 202.

Cloern, J. E., and F. H. Nichols. 1985. Time scales and mechanisms of estuarine vari- ability, a synthesis from studies of San Francisco Bay. Hydrobiologia 129:229- 237.

Cohen, A. N., and J. T . Carlton. 1998. Accelerating invasion rate in a highly invaded estuary. Science (Washington, D.C.) 279:555-558.

Conomos, T . J. 1979. Properties and circula- tion of San Francisco Bay waters. Pages 47-84 in San Francisco Bay: The urban- ized estuary. American Association for the Advancement of Science, Pacific Division, San Francisco.

Conomos, T. J., R. E. Smith, and J. W. Gartner. 198 5. Environmental setting of San Francisco Bay. Hydrobiologia 129:l- 12.

Decho, A. W., and S. N. Luoma. 1991. Time-courses in the retention of food ma-

•Influence of Hydrologic Processes on Potamocorbula amurensis . Parchaso and Thompson 343

P. amurensis larvae are capable of surviving alarge range in salinity and temperature (Ni­colini and Penry 2000). Thus, it is likely thatonce P. amurensis settled into San FranciscoBay, its ability to (1) utilize locally available,but varying sources of food resources tomaximize reproductive activity, (2) withstandand reproduce during wide changes in salinityand temperature, and (3) survive as a larva ina wide range of salinities and temperaturesallowed P. amurensis to produce many larvaeand establish a continuing presence in thebenthic community of San Francisco Bay.

ACKNOWLEDGMENTS

We gratefully acknowledge Cindy Brown,Thomas Duda, Oscar Mace, Scott Shapley,and Michelle Shouse for their assistance inthe field; Byron Richards and Scott Conard ofthe RN Polaris; and Dave Menaugh and hiscrew for their histology work. We thank SamLuoma, Fred Nichols, and two anonymousreviewers for reviewing this work.

Literature Cited

Alpine, A. E., and J. E. Cloern. 1992 . Trophicinteractions and direct physical effectscontrol phytoplankton biomass and pro­duction in an estuary. Limnol. Oceanogr.37:946-955.

Baylosis, ]. 1.,]. L. Edmunds, B. E. Cole, andJ. E. Cloern. 1997. Studies of the SanFrancisco Bay, California estuarine eco­system: Pilot regional monitoring results,1996. U.S. Geological Survey Open-FileReport 97-598.

Baylosis, ]. 1., B. E. Cole, and]. E. Cloern.1998. Studies of the San Francisco Bay,California estuarine ecosystem: Regionalmonitoring results, 1997. U.S. GeologicalSurvey Open-File Report 98-168.

Buchanan, P. A. 1999. Specific conductance,water temperature and water level data,San Francisco Bay, California, water year1998. IEP (Interagency Ecol. Program)Newsl. 14 (4): 46.

Caffrey, ]. M., B. E. Cole,]. E. Cloern,]. R.Rudek, A. C. Tyler, and A. D. Jassby.1994. Studies of the plankton and its envi-

ronment in the San Francisco Bay Estuary,California: Regional monitoring results,1993. U.S. Geological Survey Open-FileReport 94-82.

California Department of Water Resources.1999. California data exchange center(http://cdec.water.ca.gov/).

Canuel, E. A., and]. E. Cloern. 1996. Re­gional differences in the origins of organicmatter in the San Francisco Bay ecosys­tem. Pages 305-324 in]. T. Hollibaugh,ed. San Francisco Bay: The ecosystem.American Association for the Advance­ment of Science, Pacific Division, SanFrancisco.

Carlton, ]. T, ]. K. Thompson, L. E. Sche­mel, and F. H. Nichols. 1990. Remarkableinvasion of San Francisco Bay (California,USA) by the Asian clam Potamocorbulaamurensis. 1. Introduction and dispersal.Mar. Ecol. Prog. Ser. 66:81-94.

Cayan, D. R, D. H. Peterson, L. Riddle, M.D. Dettinger, and R Smith. 1997. Springrunoff pulse from the Sierra Nevada. IEP(Interagency Ecol. Program) News!' 10(3): 25-28.

Cloern,]. E. 1982. Does the benthos controlphytoplankton biomass in South San Fran­cisco Bay? Mar. Ecol. Prog. Ser. 9:191­202.

Cloern,]. E., and F. H. Nichols. 1985. Timescales and mechanisms of estuarine vari­ability, a synthesis from studies of SanFrancisco Bay. Hydrobiologia 129:229­237.

Cohen, A. N., and ]. T Carlton. 1998.Accelerating invasion rate in a highlyinvaded estuary. Science (Washington,D.C.) 279:555-558.

Conomos, T]. 1979. Properties and circula­tion of San Francisco Bay waters. Pages47-84 in San Francisco Bay: The urban­ized estuary. American Association for theAdvancement of Science, Pacific Division,San Francisco.

Conomos, T ]., R E. Smith, and ]. W.Gartner. 1985. Environmental setting ofSan Francisco Bay. Hydrobiologia 129:1­12.

Decho, A. W., and S. N. Luoma. 1991.Time-courses in the retention of food ma-

PACIFIC SCIENCE . July 2002 . terial in the bivalves Potamocorbula amur- ensis and Macoma balthica: Significance to the absorption of carbon and chromium. Mar. Ecol. Prog. Ser. 78:303-314.

Duda, T . F. 1992. Genetic population struc- ture of Potamocorbula amurensis in San Francisco Bay. M.S. thesis, San Francisco State University, San Francisco.

Edmunds, J. L., B. E. Cole, J. E. Cloern, J. M. Cafiey, and A. D. Jassby. 1995. Studies of the San Francisco Bay, California, es- tuarine ecosystem: Pilot regonal monitor- ing program results, 1994. U.S. Geological Survey Open-File Report 95-378.

Edmunds, J. L., B. E. Cole, J. E. Cloern, and R. G. Dufford. 1997. Studies of the San Francisco Bay, California, estuarine eco­system: Pilot regional monitoring program results, 1995. U.S. Geologcal Survey Open-File Report 97- 15.

Giese, A. C., and J. S. Pearse. 1974. Repro- duction of marine invertebrates. Vol. 1. Introduction: General principles. Academic Press, New York.

. 1979. Reproduction of marine in- vertebrates. Vol. 5. Molluscs: Pelecypods and lesser classes. Academic Press, New York.

Hollibaugh, J. T., and P. S. Wong. 1996. Distribution and activity of bacteri­oplankton in San Francisco Bay. Pages 263-288 in J. T . Hollibaugh, ed. San Francisco Bay: The ecosystem. Ameri- can Association for the Advancement of Science, Pacific Division, San Francisco.

Jassby, A. D., and J. E. Cloern. 2000. Organic matter sources and rehabilitation of the Sacramento-San Joaquin Delta (Califor- nia, USA). Aquat. Conserv. Mar. Fresh- water Ecosyst. 10:323-352.

Jassby, A. D., J. E. Cloern, and T. M. Powell. 1993. Organic carbon sources and sinks in San Francisco Bay: Variability induced by river flow. Mar. Ecol. Prog. Ser. 95:39- 54.

Kimmerer, W. J., E. Gartside, and J. J. Orsi. 1994. Predation by an introduced clam as the likely cause of substantial declines in zooplankton in San Francisco Bay. Mar. Ecol. Prog. Ser. 1 l3:81-93.

Lehman, P. 1996. Changes in chlorophyll a

concentration and phytoplankton commu- nity composition with water-year type in the upper San Francisco Estuary. Pages 351-374 in J. T . Hollibaugh, ed. San Francisco Bay: The ecosystem. Ameri- can Association for the Advancement of Science, Pacific Division, San Francisco.

Levine, J. M. 2000. Species diversity and bi- ologcal invasions: Relating local process to community patterns. Science (Washing- ton, D.C.) 288:852-854.

Murrel, M. C., J. T . Hollibaugh, M. W. Silver, and P. S. Wong. 1999. Bacterio- plankton dynamics in northern San Fran- cisco Bay: Role of particle association and seasonal freshwater flow. Limnol. Ocean- ogr. 44:295-308.

Nichols, F. H. 1985. Increased benthic graz- ing: An alternative explanation for low phytoplankton biomass in northern San Francisco Bay during the 1976-1977 drought. Estuarine Coastal Shelf Sci. 21: 379-388.

Nichols, F. H., J. K. Thompson, and L. E. Schemel. 1990. Remarkable invasion of San Francisco Bay (California, USA) by the Asian clam Potamocorbula amurensis. 11. Displacement of a former community. Mar. Ecol. Prog. Ser. 66:95-101.

Nicolini, M. H., and D. L. Penry. 2000. Spawning, fertilization, and larval devel- opment of Potamocorbula amurensis (Mol­lusca: Bivalvia) from San Francisco Bay, California. Pac. Sci. 54:3 77-3 88.

Parchaso, F. 1995. Seasonal reproduction of Potamocorbula amurensis in San Francisco Bay, California. M.S. thesis, San Francisco State University, San Francisco.

Rosenblum, S., and T. M. Niesen. 1985. The spawning cycle of soft-shell clam Mya arenaria in San Francisco Bay. Fish. Bull. 83:403-412.

Ruhl, C. A., and D. H. Shoelhammer. 1997. Time series of suspended-solids concen- tration in Honker Bay during water year 1997. San Francisco Estuary Institute, 1997 Regional Monitoring Program An- nual Report.

Schemel, L. E., S. W. Hager, and D. Child- ers. 1996. The supply of suspended sedi- ment from the Sacramento River to San

344

terial in the bivalves Potamocorbula amur­ensis and Macoma balthica: Significance tothe absorption of carbon and chromium.Mar. Ecol. Prog. Ser. 78:303-314.

Duda, T F. 1992. Genetic population struc­ture of Potamocorbula amurensis in SanFrancisco Bay. M.S. thesis, San FranciscoState University, San Francisco.

Edmunds, ]. L., B. E. Cole, ]. E. Cloern, ].M. Caffrey, and A. D.Jassby. 1995. Studiesof the San Francisco Bay, California, es­tuarine ecosystem: Pilot regional monitor­ing program results, 1994. U.S. GeologicalSurvey Open-File Report 95-378.

Edmunds,]. L., B. E. Cole,]. E. Cloern, andR. G. Dufford. 1997. Studies of the SanFrancisco Bay, California, estuarine eco­system: Pilot regional monitoring programresults, 1995. U.S. Geological SurveyOpen-File Report 97-15.

Giese, A. C, and]. S. Pearse. 1974. Repro­duction of marine invertebrates. Vol. 1.Introduction: General principles. AcademicPress, New York.

---. 1979. Reproduction of marine in­vertebrates. Vol. 5. Molluscs: Pelecypodsand lesser classes. Academic Press, NewYork.

Hollibaugh, ]. T, and P. S. Wong. 1996.Distribution and activity of bacteri­oplankton in San Francisco Bay. Pages263-288 in ]. T Hollibaugh, ed. SanFrancisco Bay: The ecosystem. Ameri­can Association for the Advancement ofScience, Pacific Division, San Francisco.

Jassby, A. D., and]. E. Cloern. 2000. Organicmatter sources and rehabilitation of theSacramento-San Joaquin Delta (Califor­nia, USA). Aquat. Conserv. Mar. Fresh­water Ecosyst. 10:323-352.

Jassby, A. D.,]. E. Cloern, and T M. Powell.1993. Organic carbon sources and sinks inSan Francisco Bay: Variability induced byriver flow. Mar. Ecol. Prog. Ser. 95:39­54.

Kimmerer, W.]., E. Gartside, and].]. Orsi.1994. Predation by an introduced clam asthe likely cause of substantial declines inzooplankton in San Francisco Bay. Mar.Ecol. Prog. Ser. 113:81-93.

Lehman, P. 1996. Changes in chlorophyll a

PACIFIC SCIENCE· July 2002

concentration and phytoplankton commu­nity composition with water-year type inthe upper San Francisco Estuary. Pages351-374 in ]. T Hollibaugh, ed. SanFrancisco Bay: The ecosystem. Ameri­can Association for the Advancement ofScience, Pacific Division, San Francisco.

Levine, ]. M. 2000. Species diversity and bi­ological invasions: Relating local process tocommunity patterns. Science (Washing­ton, D.C) 288:852-854.

Murrel, M. C, ]. T Hollibaugh, M. W.Silver, and P. S. Wong. 1999. Bacterio­plankton dynamics in northern San Fran­cisco Bay: Role of particle association andseasonal freshwater flow. Limnol. Ocean­ogr. 44:295-308.

Nichols, F. H. 1985. Increased benthic graz­ing: An alternative explanation for lowphytoplankton biomass in northern SanFrancisco Bay during the 1976-1977drought. Estuarine Coastal Shelf Sci. 21:379-388.

Nichols, F. H., ]. K. Thompson, and L. E.Schemel. 1990. Remarkable invasion ofSan Francisco Bay (California, USA) bythe Asian clam Potamocorbula amurensis. II.Displacement of a former community.Mar. Ecol. Prog. Ser. 66:95-101.

Nicolini, M. H., and D. L. Penry. 2000.Spawning, fertilization, and larval devel­opment of Potamocorbula amurensis (Mol­lusca: Bivalvia) from San Francisco Bay,California. Pac. Sci. 54:377-388.

Parchaso, F. 1995. Seasonal reproduction ofPotamocorbula amurensis in San FranciscoBay, California. M.S. thesis, San FranciscoState University, San Francisco.

Rosenblum, S., and T M. Niesen. 1985. Thespawning cycle of soft-shell clam Myaarenaria in San Francisco Bay. Fish. Bull.83:403-412.

Rubl, C A., and D. H. Shoelhammer. 1997.Time series of suspended-solids concen­tration in Honker Bay during water year1997. San Francisco Estuary Institute,1997 Regional Monitoring Program An­nual Report.

Schemel, L. E., S. W. Hager, and D. Child­ers. 1996. The supply of suspended sedi­ment from the Sacramento River to San

Influence of Hydrologic Processes on Potumocorbula amurensis . Pnrrhuso und Thompson 345 6

Francisco Bay. Pages 217-235 in J. T . Hollibaugh, ed. San Francisco Bay: The ecosystem. American Association for the Advancement of Science, Pacific Division, San Francisco.

Thompson, J. K., L. E. Schemel, F. H. Nichols, and J. T. Carlton. 1988. The in- vasion of San Francisco Bay by the bivalve Potamocorbula. Am. Zool. 2 8:3 59.

Varon, S. C. 1978. The population distribu- tion and reproductive cycle of Tapes japon- ica. M.S. thesis, San Francisco State University, San Francisco.

Walters, R. A., R. T. Cheng, and T . J. Con­omos. 1985. Time scales and mixing pro- cesses of San Francisco Bay waters. Hydrobiologia l29:13-16.

Werner, I., and J. T. Hollibaugh. 1993. Pota­mocorbula amurensis: Comparison of clear- ance rates and assimilation efficiencies for phytoplankton and bacterioplankton. Lim- nol. Oceanogr. 38:949-964.

Wienke, S. M., J. E. Cloern, and B. E. Cole. 1990. Plankton studies in San Francisco Bay. XI. Chlorophyll distributions and hy-

drographic properties in San Francisco Bay, 1988-1989. U.S. Geological Survey Open-File Report 90-562.

Wienke, S. M., B. E. Cole, J. E. Cloern, and A. E. Alpine. 1991. Plankton studies in San Francisco Bay. XII. Chlorophyll distribu- tions and hydrographic properties in San Francisco Bay, 1990. U.S. Geological Sur- vey Open-File Report 91-476.

. 1992. Plankton studies in San Fran- cisco Bay. XIII. Chlorophyll distributions and hydrographic properties in San Fran- cisco Bay, 1991. U.S. Geological Survey Open-File Report 92-158.

. 1993. Plankton studies in San Fran- cisco Bay. X I V . Chlorophyll distributions and hydrographic properties in San Fran- cisco Bay, 1992. U.S. Geological Survey Open-File Report 93-42 3.

Wilson, B. R. 1969. Survival and reproduc- tion of the mussel Xenostrobus securis (La­marck) (Mollusca; Bivalvia; Mpilidae) in a Western Australian estuary. Part 11: Re­production, growth and longevity. J. Nat. Hist. 3:93-120.

•Influence of Hydrologic Processes on Potamocorbula amurensis . Parchaso and Thompson 345

Francisco Bay. Pages 217-235 in ]. T.Hollibaugh, ed. San Francisco Bay: Theecosystem. American Association for theAdvancement of Science, Pacific Division,San Francisco.

Thompson, ]. K., L. E. Schemel, F. H.Nichols, and]. T. Carlton. 1988. The in­vasion of San Francisco Bay by the bivalvePotamocorbula. Am. Zool. 28:359.

Varon, S. C. 1978. The population distribu­tion and reproductive cycle of Tapes japon­ica. M.S. thesis, San Francisco StateUniversity, San Francisco.

Walters, R. A., R. T. Cheng, and T.]. Con­omos. 1985. Time scales and mixing pro­cesses of San Francisco Bay waters.Hydrobiologia 129:13-16.

Werner, I., and]. T. Hollibaugh. 1993. Pota­mocorbula amurensis: Comparison of clear­ance rates and assimilation efficiencies forphytoplankton and bacterioplankton. Lim­nol. Oceanogr. 38:949-964.

Wienke, S. M.,]. E. Cloern, and B. E. Cole.1990. Plankton studies in San FranciscoBay. XI. Chlorophyll distributions and hy-

drographic properties in San FranciscoBay, 1988-1989. U.S. Geological SurveyOpen-File Report 90-562.

Wienke, S. M., B. E. Cole,]. E. Cloem, andA. E. Alpine. 1991. Plankton studies in SanFrancisco Bay. XII. Chlorophyll distribu­tions and hydrographic properties in SanFrancisco Bay, 1990. U.S. Geological Sur­vey Open-File Report 91-476.

~~-. 1992. Plankton studies in San Fran­cisco Bay. XIII. Chlorophyll distributionsand hydrographic properties in San Fran­cisco Bay, 1991. U.S. Geological SurveyOpen-File Report 92-158.

~~-. 1993. Plankton studies in San Fran­cisco Bay. XIV. Chlorophyll distributionsand hydrographic properties in San Fran­cisco Bay, 1992. U.S. Geological SurveyOpen-File Report 93-423.

Wilson, B. R. 1969. Survival and reproduc­tion of the mussel Xenostrobus securis (La­marck) (Mollusca; Bivalvia; Mytilidae) in a\Vestern Australian estuary. Part II: Re­production, growth and longevity. ]. Nat.Hist. 3:93-120.