Spatial and overwinter changes in clam populations of San Pablo Bay, a semiarid estuary with highly variable freshwater inflow

Estuarine, Coastal and Shelf Science 59 (2004) 459e473

Spatial and overwinter changes in clam populations of San Pablo Bay, a semiarid estuary with highly variable freshwater inflow V.K. Poultona,1, J.R. Lovvorna,), J.Y. Takekawab a Department of Zoology, University of Wyoming, P.O. Box 3166, Laramie, WY 82071, USA U.S. Geological Survey, Western Ecological Research Center, San Francisco Bay Estuary Field Station, P.O. Box 2012, Vallejo, CA 94592, USA

b

Received 20 December 2002; accepted 16 October 2003

Abstract In many estuaries worldwide, climate trends together with human diversion of fresh water have dramatically impacted the benthos. Such impacts have sometimes been complicated by exotic species, whose invasion and persistence can be mediated by wide variations in freshwater inflow. Monitoring such changes usually involves periodic samples at a few sites; but sampling that does not recognize variation at a range of spatial and seasonal scales may not reveal important benthic trends. San Pablo Bay, in northern San Francisco Bay, has extreme fluctuations in freshwater inflow. This bay also experienced a major benthic change with introduction of the Asian clam (Potamocorbula amurensis) in 1986. This species initially displaced the former community, but later appeared to vary in abundance depending on site and freshwater inflow. To investigate such patterns and provide guidelines for research and monitoring, we took 1746 core samples at six sites around San Pablo Bay from 19 October to 17 December 1999 and from 6 March to 19 April 2000. Most biomass consisted of the clams P. amurensis, Macoma balthica and Mya arenaria. Potamocorbula amurensis dominated the benthos at most sites in the fall and recruited a new cohort during winter, while there was weak recruitment in M. balthica and none in M. arenaria. At most but not all sites, densities of P. amurensis and M. arenaria declined dramatically over winter while M. balthica declined only slightly. The dominant clams had patch diameters O5 m at most but not all sites, and some showed inconsistent patch structure at scales of 100e1400 m. In this semiarid estuary with highly variable freshwater inflow, samples for research and monitoring should include multiple sites and seasons, and samples within sites should be R5 m apart to account for between-patch variation. Species abundance in winter 1999e2000 appeared to be affected by high freshwater inflows in 1997e1999, while spatial patterns were probably most affected by post-settlement dispersal and mortality. Ó 2003 Elsevier Ltd. All rights reserved. Keywords: benthic macroinvertebrates; freshwater inflow; Macoma balthica; Mya arenaria; Potamocorbula amurensis; San Pablo Bay; spatial dispersion

1. Introduction In many estuaries worldwide, climate variations coupled with human diversion of fresh water have caused important changes in biotic communities (Brad1 Present address: South Slough National Estuarine Research Reserve, Estuarine and Coastal Science Laboratory, P.O. Box 5417, Charleston, OR 97420, USA. ) Corresponding author. Tel.: +1-307-766-6100; fax: +1-307-7665625. E-mail address: [email protected] (J.R. Lovvorn).

0272-7714/04/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2003.10.005

ley et al., 1990; McIvor et al., 1994; Peterson et al., 1995; Attrill et al., 1996; Livingston et al., 1997; Gibson and Najjar, 2000). These changes have been especially dramatic in arid and semiarid regions where precipitation is highly variable and water diversions extreme (Cayan and Peterson, 1993; Jassby et al., 1995; Baird and Heymans, 1996; Rodriguez et al., 2001; Snyder et al., 2002). In some cases, sampling programs have been established to yield criteria for monitoring and managing freshwater inflow for native or other desirable species (Martin, 1987; Williams, 1989; Longley,

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1994; Jassby et al., 1995; Schumann and Pearce, 1997; Attrill and Power, 2000). Such sampling designs must account for seasonal and spatial variations, or else the scales of sampling can be inappropriate for the major functions of interest (Livingston, 1982; Baird and Heymans, 1996; Ardisson and Bourget, 1997; Schumann and Pearce, 1997; Wortmann et al., 1998). Thus, before designing sampling schemes, one must identify important scales of variation relative to the ecological processes studied (Livingston, 1987; Duarte and Kalff, 1990; Thrush, 1991; Hewitt et al., 1998). In the San Francisco estuary, California (Fig. 1), spatial and temporal changes in benthic fauna were described in the 1950s to 1980s (Filice, 1958; Siegfried et al., 1980; Nichols and Thompson, 1985a,b; Nichols and Pamatmat, 1988). Despite high variation with fluctuating freshwater inflow, species composition generally remained similar over the long term except for invasion by exotic species. One such species, the Asian clam (Potamocorbula amurensis), invaded in 1986e1987 and quickly spread throughout the bay, largely displacing the former clam assemblage (Carlton et al., 1990; Nichols et al., 1990). More recently, this species’

Fig. 1. San Pablo Bay, located in northern San Francisco Bay, California (inset) with the six sampling sites shown: MI, Mare Island; He, Hercules; Ca, Castro Cove; SQ, San Quentin; CC, China Camp; BM, Bel Marin. Shaded areas are !2 m deep at Mean Lower Low Water.

abundance relative to resident clams appears to have fluctuated depending on site and freshwater inflow. Most benthic research and monitoring have been done in the South Bay, a polysaline, lagoon-type embayment with little fluvial influence except in wet years, and in Suisun Bay, a mostly oligosaline embayment in the upper estuary (Fig. 1). San Pablo Bay differs from the South and Suisun Bays in having a relatively broader area !2 m deep and much greater variations in salinity (Knowles, 2000; see also http://tenaya.ucsd.edu/ wknowles/papers/pred/pred01.html). Although San Pablo Bay has been much less studied, it is the most important wintering area for most diving ducks on the North American Pacific coast (Accurso, 1992), and provides key wintering or nursery habitat for valued fish and shellfish such as sturgeon, sole and crabs (Ganssle, 1966; Tasto, 1979; Armor and Herrgesell, 1985; Kohlhorst et al., 1991). The benthic community of San Pablo Bay reflects annual and seasonal salinities determined by freshwater inflow from the semiarid Sacramento-San Joaquin Delta (Nichols and Thompson, 1985b). During low flows and high salinities, marine species such as the amphipod Ampelisca abdita and the soft-shelled clam Mya arenaria have been found throughout San Pablo Bay and up into Suisun Bay. When river inflows are high and salinity is low, freshwater species such as the clam Corbicula fluminea can move downstream while A. abdita disappears from the upper reaches of the estuary (Nichols and Thompson, 1985b). The exotic Potamocorbula amurensis is euryhaline and can tolerate nearly fresh water (Nicolini and Penry, 2000). Early reports indicated that P. amurensis did not move up and down the estuary with varying freshwater inflow as did other clams in San Pablo Bay, making it a dominant colonizer and competitor (Nichols et al., 1990). The magnitude and timing of phytoplankton blooms in this estuary depend on freshwater inflow. As in Suisun Bay just upstream, blooms in San Pablo Bay may be larger when freshwater inflow places the null zone in the main channel adjacent to large areas of shallow water (Ball and Arthur, 1979; Cloern, 1979; Williams and Hollibaugh, 1987; Jassby et al., 1996). In San Pablo Bay, highest chlorophyll a concentrations usually occur between April and June. Many benthic invertebrates in San Pablo Bay reproduce in spring and depend on phytoplankton blooms for food during spawning and growth (Thompson, 1982; Kinnetic Laboratories, 1983; Rosenblum and Niesen, 1985; Thompson and Nichols, 1988; Parchaso, 1995). Thus, spatial and seasonal patterns of the San Pablo Bay benthos merit greater study and consideration in plans to regulate freshwater inflow. We focused on clams used as prey by diving ducks, especially Lesser and Greater Scaup (Aythya affinis, Aythya marila) (Poulton et al., 2002). Spatial variation

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in prey is important to food availability for these benthivores. For subterranean tubers of the submersed plant Vallisneria americana eaten by congeneric Canvasback ducks (Aythya valisineria), Lovvorn and Gillingham (1996) detected no predictable patch structure at scales of 0 to 6 m in a shallow lake in North Carolina. However, bivalves often exhibit patchy distributions in soft sediments (Gage and Geekie, 1973; Schneider, 1987; Thrush, 1991; Thompson, 1999). Given the variation in feeding mode and burial depth among bivalve species in San Pablo Bay, we expected differences in dispersion of those species. For example, clumped distributions at small scales may not persist at larger scales, because the water layer advected over bigger patches of clams can become depleted of particulate food (Thompson, 1999). Moreover, Macoma balthica is a facultative depositfeeder and can probably exploit foods unavailable to filter-feeding Mya arenaria or Potamocorbula amurensis. With longer siphons, M. balthica and M. arenaria can also burrow deeper than P. amurensis, and may be less subject to redistribution by scouring (Roegner et al., 1995). In this study, we measured the size and abundance of the main prey for scaup and investigated how bivalve prey varied among and within important feeding sites across the wintering period. We also examined the patch structure of different species at different sites, to guide appropriate spacing and extent of samples. Consequently, in 1999e2000, we sampled at multiple spatial scales throughout this area in late fall and early spring, times that coincide with the arrival and departure, respectively, of scaup. This study provided short-term, spatially comprehensive data to complement longer-term but spatially more limited data from other studies in San Pablo Bay (e.g., Nichols and Thompson, 1985b).

2.2. Benthic sampling At each site (Fig. 1), a single transect was established where the water was 0.3e3 m deep at Mean Lower Low Water. We selected transect locations arbitrarily at high tide when water obscured any benthic features that might bias our choice, thus approximating randomness. Transects were perpendicular to shoreline, and 360e1400 m long depending on the width of the area spanning these depths. Triplicate subsamples were taken within 1 m of each other at stations spaced equidistantly along each transect: 10 stations over 360 m at Hercules, 15 stations over 1120 m at Mare Island and San Quentin, and 15 stations over 1400 m at Bel Marin, Castro Cove and China Camp. Samples were taken to a depth of 20 cm below the sediment surface with a winch-deployed, stainless steel corer 10 cm in diameter. (See Poulton et al., 2002, for results from sediment layers shallower than 20 cm.) The same stations along the main transects (Fig. 2) were sampled in the fall from 19 October to 17 December 1999 and in the spring from 6 March to 19 April 2000. During the fall period, additional triplicate samples were taken at 1-m increments to a distance of 5 m downwind from each station (Fig. 2); these samples were used in analyses of patch structure. Core samples were stored in plastic zip-lock bags and either processed after collection or frozen and later thawed for processing. Samples were sieved through a 1-mm mesh (rather than 0.5-mm mesh) to reduce sieving time, thereby allowing us to handle our

Station 15

2. Methods

San Pablo Bay (Fig. 1) has a surface area of 215 km2, roughly two-thirds of which is !2 m deep. Salinity at the upstream end of San Pablo Bay can vary from 2 during spring runoff to 23 at low inflows in late summer (salinities according to the Practical Salinity Scale; Nichols, 1979; Conomos et al., 1985). Sediments are mostly clay, silt, and some sand (Conomos et al., 1985), and the water in this shallow windy area is very turbid. For benthic sampling, our main concern was prey availability for scaup (Poulton et al., 2002). Based on movements of radio-tagged scaup (J. Y. Takekawa, unpubl. data), we identified six sites around San Pablo Bay, including one site in nearby San Quentin Bay, that were heavily used by scaup and readily accessible by boat (Fig. 1).

Station 3 Wind Direction

Station 2

Station 1 Me ter 0 Me ter 1 Me ter 2 Me ter 3 Me ter Me 4 ter 5

2.1. Study area

461

Shoreline

Fig. 2. Diagram of transect layout and core sampling pattern used in fall 1999 to investigate spatial dispersion of benthic invertebrates. In spring 2002, samples were taken at the same stations along the main transect line, without the additional samples at increments of 1 m. Solid circles represent single core subsamples.

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very large number of core samples (n ¼ 1746). All clams retained by the 1-mm sieve were identified to species and their shell length measured to the nearest 0.5 mm. Other retained invertebrates were identified to varying taxonomic levels. The number of individuals was averaged over each triplicate set of subsample cores. Our sampling unit of interest was an area comprising the locus of a foraging dive by a duck (w1 m in diameter), which is likely to be the smallest ‘‘grain’’ or first order of patchiness to which they respond (Lovvorn and Gillingham, 1996). Because the area sampled by our corer (79 cm2) was much smaller than a foraging locus, we took three subsamples to capture more of the variability in such an area. We did not attempt to measure patchiness on a scale !1 m, as it would not have been relevant to our objectives. We sampled using a corer with a long handle in water usually 0.5 to 1.5 m deep. As depicted in Fig. 2, there was almost always a breeze that maintained the orientation of the anchored boat while we sampled at a given station, so that paying out known amounts of anchor rope allowed consistent placement of replicate cores for each 1-m interval. For cross-seasonal comparisons, mean density per station in spring 2000 was the mean for a single triplicate set of cores, whereas in fall 1999, mean density per station was calculated as the mean of the six triplicate samples taken at 1-m increments at each station. For sediment analyses, one core (10 cm diameter, 20 cm deep) was taken at each station on each transect (excluding sample locations at 1-m increments downwind of each station) and frozen until processed. The entire core was homogenized, and particle-size fractions were determined from oven-dried subsamples by soaking a 5-g portion in a dispersal agent (Calgon water softener) and wet-sieving to remove the silteclay fraction (!0.063 mm). The subsample was then dried again and the silteclay fraction determined by loss of mass. The fraction O0.063 mm was then passed through a series of sieves with mesh sizes of 2.0, 0.5, 0.25 and 0.125 mm and the fraction retained on each sieve was weighed. Each size fraction was determined as a percentage of the original subsample mass. For regressions against invertebrate densities, sediment size fractions were combined into coarse (R0.5 mm), medium (!0.5 and R0.063 mm), and silteclay (!0.063 mm) fractions. Organic matter content was determined by loss of mass on ignition at 500 (C for 8 h. 2.3. Statistics, dispersion index and autocorrelation Data were ln(x þ 1)-transformed where appropriate to meet assumptions of normality and homoscedasticity. If the data still did not meet the assumptions, ranktransformations were used for nonparametric tests. Clam densities (by species) were compared between

seasons and transects by nested ANOVA with Bonferroni t-tests (three replicate cores nested within meter, station, and transect; MINITAB, Inc., State College, Pennsylvania, U.S.A.). Sediment organic matter was compared between seasons and transects by ANOVA with Bonferroni t-tests (PROC GLM, SAS Institute, Cary, North Carolina, U.S.A.). Despite differing numbers of cores in fall versus spring (Fig. 2), statistical comparisons between seasons were valid because the dependent variable was the mean number of clams m
2 for each station on the transect. Sediment size fractions were compared between seasons and transects using MANOVA (PROC MANOVA, SAS). Effects of sediment characteristics on clam densities were investigated with multiple least-squares regression, and important predictor variables were chosen by stepwise model selection (MINITAB, Inc.). In this paper, r2 values are reported with a negative sign if there is a negative relationship between variables. Dispersions of the most abundant clams (Potamocorbula amurensis, Macoma balthica and Mya arenaria) were evaluated using Green’s Index, defined as GI ¼ ðs2 = xÞ
½1=ðN
1Þ, where N is the number of samples taken along the transect at a given site (each sample value was the mean of three replicate cores), and x and s2 are the mean and variance of density among stations at that site (Ludwig and Reynolds, 1988). GI varies from
1=ðN
1Þ for maximum uniformity to 0 for randomness to +1 for maximum clumping. For the fall data, patch structure was investigated via spatial autocorrelation by testing whether the number of a clam species at one sample location (one set of triplicate cores) was independent of numbers in neighboring sample locations. Data for autocorrelation analyses were collected by taking triplicate cores at 1-m increments to a distance of 5 m in the downwind direction from each station along the transect at a given site (Fig. 2). These data were treated as if taken in an irregular lattice (Sawada, 1999). Correlograms were created for clam density on a small scale of 1 to 5 m (lag distance = 1 m, number of lags = 5), and on a large scale between 100 m and the length of the transect (360e1400 m) (lag distance = 100 m, number of lags = 4e14). Note that patch structure at intermediate scales between 5 and 100 m could not be detected by our design. Instead, our sampling was intended to detect variations in small-scale patch structure at foraging sites used by benthic predators that tend to move relatively large distances between such foraging sites (Poulton et al., 2002). Moran’s I was calculated as P N ij wij zi zj I¼ ð1Þ PN W i¼1 z2i P where N = number of sample locations, ij = summation over all ij from i ¼ 1 to N and j ¼ 1 to N for isj,

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wij = binary weight (0 or 1) of whether two locations are adjacent (neighbors) at the minimum scale (lag distance) specified, zi ¼ gi
g where gi is the value of variable g for location i and g is the mean of g for all locations, and W = sum of the binary weights in the adjacency matrix = twice the number of distances connecting all sample locations (Sokal and Oden, 1978). We used a Visual Basic add-in for Microsoft Excel (Sawada, 1999) to calculate Moran’s I. Values for Moran’s I range from
1 for neighboring values with maximal difference to +1 for neighboring values with maximal similarity; a value of 0 indicates no autocorrelation. For example, negative Moran’s I values at distances of 1, 2 and 3 m between sampling stations indicate that densities at all stations 1, 2 or 3 m apart are on average negatively correlated. Conversely, positive Moran’s I values would indicate positive correlations between stations at these distances apart. The significance of Moran’s I for each distance between samples as incremented by the lag distance (e.g., 1, 2, 3, 4 and 5 m at the small scale examined) was determined by z-tests with Bonferroni correction, i.e., using a/k for each test, where k = the number of distances being tested within a given range (Legendre and Fortin, 1989).

3. Results We collected 514 triplicate samples (1542 cores) in fall 1999 and 68 triplicate samples (204 cores) in spring 2000. At Bel Marin in the spring, sediment samples were taken but invertebrate samples were not, owing to overwinter sediment deposition that impeded access by boat. The most abundant taxa were polychaetes and the bivalves Potamocorbula amurensis, Macoma balthica and Mya arenaria; amphipods were important only at some sites

and seasons (Table 1). No Ampelisca abdita amphipods or Gemma gemma clams were collected despite past reports that these species were common in this area (Nichols and Thompson, 1985b). 3.1. Effects of site, season and sediments Invertebrate density varied widely among sites and seasons, although densities at the nested sampling level of replicate and meter were more similar (Tables 1 and 2; Fig. 3). Three bivalves occurred in sufficient numbers for more detailed comparisons. Density (number m
2) of Potamocorbula amurensis declined dramatically from fall to spring at all sites except Castro Cove where they increased in spring (Fig. 3). Macoma balthica densities changed significantly only at China Camp and Hercules, where declines were much smaller than for P. amurensis. Mya arenaria decreased significantly between fall and spring at the three sites where they were found. Fewer clams were collected in spring due to reduced clam densities and collection of fewer cores. However, a new size class for Potamocorbula amurensis, indicating recruitment between fall and spring sampling, was clearly evident at Castro Cove and perhaps at China Camp and Mare Island, although only two individuals were in the new size class at China Camp (Fig. 4). For Macoma balthica there was no clear evidence of recruitment except perhaps at Mare Island. Mya arenaria did not recruit between fall and spring. Sediments were composed mostly of silt and clay (!0.063 mm), although sites varied in proportions of larger particles (MANOVA, Wilks’ l ¼ 0:36, F25;510 ¼ 0:66, P!0:001, Fig. 5). Sediment grain size did not vary within sites between fall and spring (MANOVA, Wilks’ l ¼ 0:98, F5;137 ¼ 0:98, P ¼ 0:658). Most particles O0.063 mm were mollusk shell fragments. Organic matter content of sediments did not change between seasons

Table 1 Average density (individuals m
2) of invertebrates retained by a 1-mm sieve at six sites in San Pablo Bay, California during fall (19 Octobere17 December 1999) and spring (6 Marche9 April 2000) Species

BM

Ca

CC

He

MI

SQ

Fall Potamocorbula amurensis Macoma balthica Mya arenaria Polychaetes Amphipods

158.0 103.7 tr 53.2 tr

124.0 tr 66.9 18.3 0

66.8 32.6 2.8 74.3 129.4

657.7 56.7 99.7 64.9 53.6

417.9 112.7 tr 5.6 0

36.2 11.2 119.7 77.2 0

223.6 0 14.1 11.2 223.4

6.5 13.0 0 88.3 0

0 34.0 0 29.7 0

87.7 124.6 0 0 0

tr tr

Spring Potamocorbula amurensis Macoma balthica Mussels Polychaetes Amphipods

0 tr tr

Invertebrates were not sampled at Bel Marin in spring. When !10 individuals were found along an entire transect, the density is indicated as trace (tr). Taxa that never occurred in greater than trace amounts are not listed. BM, Bel Marin; Ca, Castro Cove; CC, China Camp; He, Hercules; MI, Mare Island; SQ, San Quentin (Fig. 1).

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Table 2 Results of nested ANOVA (three replicate cores; nesting within meter, station and site indicated by parentheses) with interaction of season ! site for ln(x þ 1)-transformed densities of Macoma balthica and Potamocorbula amurensis, and rank-transformed densities of Mya arenaria, in San Pablo Bay, California. See Table 1 for un-transformed means Species

Factor

df

F

P-value

Macoma balthica

Season Site Station (site) Meter (site, station) Replicate (site, station, meter) Season ! transect

1 4 65 353 846 4

5.9 34.1 4.0 0.9 0.8 1.5

0.02 !0.001 !0.001 0.77 0.98 0.19

Potamocorbula amurensis

Season Site Station (site) Meter (site, station) Replicate (site, station, meter) Season ! transect

1 4 65 353 846 4

90.6 46.2 12.2 1.3 1.2 43.3

!0.001 !0.001 !0.001 0.01 0.12 !0.001

Mya arenaria

Season Site Station (site) Meter (site, station) Replicate (site, station, meter) Season ! transect

1 4 65 353 846 4

42.2 14.2 6.1 1.3 1.2 8.5

!0.001 !0.001 !0.001 0.04 0.09 !0.001

(ANOVA, F1;152 ¼ 1:64, P ¼ 0:203), but differed significantly among sites (F5;149 ¼ 14:4, P!0:001). Sediment organic content ranged from 2.3 to 8.7% among all sampling stations, with means for Bel Marin and China Camp 250

250

Bel Marin

-2

Density (number m )

200

not sampled in spring

200

150

150

100

100

50

50

0

0

250

800

*

Hercules 700

150

50

Castro Cove

China Camp

200

100

*

*

600 200

*

*

100

0

0

500

250

*

Mare Island

*

San Quentin

200

400

*

150

200

*

100

100

50

0

0

Pa

Mb

Ma

* Pa

being higher than for all other sites, and the mean for San Quentin being higher than for Castro Cove (Fig. 5). Invertebrate densities were correlated with sediment grain size and organic matter content. Potamocorbula amurensis densities (mean number in 3 cores/station combined, N ¼ 83 stations in fall, 71 in spring) decreased slightly with increasing organic matter content in the fall (r2 ¼
0:06, P!0:001) and in the spring (r2 ¼
0:05, P ¼ 0:04). Potamocorbula amurensis densities increased with higher silteclay fraction in the fall (r2 ¼ 0:09, P ¼ 0:007) but not in the spring. For Macoma balthica, densities were not affected by sediment grain size or organic matter content in the fall; but in the spring, densities decreased with increasing organic content of sediments (r2 ¼ 0:10, P!0:001) and increased with increasing silteclay content (r2 ¼ 0:26, P!0:001). Mya arenaria densities in the fall had a weak positive association with increasing organic matter content (r2 ¼ 0:03, P ¼ 0:08), decreased with increasing silteclay content (r2 ¼
0:21, P ¼ 0:001) and increased with increasing coarse sediments (r2 ¼ 0:08, P ¼ 0:009). In the spring, M. arenaria densities were not associated with sediment characteristics. 3.2. Patterns of dispersion

Mb

Ma

Species Fig. 3. Mean density (individuals m
2) of benthic invertebrates (+1 SE) at six sites around San Pablo Bay (Fig. 1) in fall 1999 (black bars) and spring 2000 (white bars). Bars marked with an asterisk are significantly different (Bonferroni pairwise comparisons by species, P!0:05). Pa, Potamocorbula amurensis; Mb, Macoma balthica; Ma, Mya arenaria.

Values of Green’s Index (GI) range from
1=ðN
1Þ for maximum uniformity to 0 for randomness to +1 for maximum clumping. Values of maximum uniformity were
0.017 (N ¼ 60 sample locations) at Hercules and
0.011 (N ¼ 90) at the other five sites (Fig. 1). For Potamocorbula amurensis, GI averaged 0.063 (range 0e0.194) for all sites, with all values except one being

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465

Fig. 4. Length frequencies of the three most common bivalves in San Pablo Bay during fall (19 Octobere17 December) 1999 and spring (6 Marche19 April) 2000. Except for Bel Marin which was not sampled in the spring, missing graphs indicate that no specimens of that species were found in the spring. Transects at different sites (Fig. 1) were sampled in the same proportions in fall and spring, but total sampling effort was reduced from 1542 cores at 514 stations in fall to 204 cores at 68 stations in spring (Fig. 2).

!0.076. Thus, P. amurensis had a mostly random to slightly clumped dispersion. GI values for Macoma balthica ( x ¼ 0:013, range
0.006e0.062) and Mya arenaria ( x ¼ 0:002, range
0.004e0.047) also indicated an essentially random dispersion.

Our sampling design allowed us to detect patch structure in the fall at two scales: a small scale of 1 to 5 m and a large scale of 100 m to the length of the transect. We could not identify the dimensions of patches between 5 and 100 m wide. At a scale of 1 to 5 m, Potamocorbula

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4. Discussion Species composition of the benthos of San Pablo Bay in winter 1999e2000 was generally similar to that in the 1980s (Nichols and Thompson, 1985a,b; Nichols and Pamatmat, 1988). However, the density and relative numbers of species varied among sites, as did patterns of change from fall to spring. In particular, densities of the recently established Potamocorbula amurensis declined dramatically over winter at most sites, while densities of Macoma balthica declined only slightly. 4.1. Patterns of Potamocorbula and Macoma

Fig. 5. Sediment particle-size fractions and organic matter content for six sites around San Pablo Bay (Fig. 1). Samples from fall 1999 and spring 2000 are combined as they were not significantly different (for particle size: MANOVA, Wilks’ l ¼ 0:98, F5;137 ¼ 0:98, P ¼ 0:658; for organic matter: ANOVA, F1;152 ¼ 1:64, P ¼ 0:203). Size fractions are based on dry mass of a 25-g subsample of sediment at each station.

amurensis showed positive autocorrelation (indicated by values significantly greater than 0) at all sites except China Camp (Fig. 6a). Most trends suggested a patch diameter R5 m, and at least 3 m at China Camp. On the larger scale, P. amurensis showed positive autocorrelation that indicated higher-order patches at 100e200 m at all sites except Bel Marin, where positive autocorrelation extended up to 400 m. At Castro Cove, Mare Island and San Quentin, higher-order patches were also indicated at 900e1000 m. The Hercules transect was not long enough to examine large-scale gradients. Macoma balthica showed a patch diameter O5 m at all sites except San Quentin, where no patchiness was detected at the small scale (Fig. 6b). Densities of M. balthica were too low at Castro Cove to investigate patch structure. On the larger scale, there was clear patchiness at 100e400 m at Bel Marin, China Camp and Mare Island, and lack of similarity at 800e1400 m. Mya arenaria occurred in high enough numbers for spatial analysis at Castro Cove, Hercules and San Quentin (Fig. 6c). Patch diameter was O5 m at the latter two sites, whereas no small-scale patch structure was evident at Castro Cove. At the larger scale, there were still no patterns at Castro Cove. Mya arenaria at Hercules showed large-scale positive autocorrelation at 100 m, and at San Quentin at 100e200 m. Mya arenaria followed a gradient of decreasing similarity at San Quentin, and such a gradient was also suggested at Hercules.

With a 1-mm sieve, the mean density of Potamocorbula amurensis during winter 1999e2000 for 582 sets of triplicate samples was 152 m
2 (range 0e1273). The highest density among 1746 triplicate cores was 2206 m
2. These values are far lower than densities of over 10,000 m
2 (average valve length 1.7 mm) in 1987e1988 based on a 0.5-mm sieve (Carlton et al., 1990), although this species was still numerically dominant in San Pablo Bay in 1999e2000. Despite its tolerance for nearly fresh water, P. amurensis may be adversely affected by high freshwater inflows because of associated scouring by water currents. In fall 1999, 96.5% of P. amurensis lived in the top 5 cm of sediments while fewer than half the Macoma balthica were in this top layer (Poulton et al., 2002). The short siphon and shallow burying depth of P. amurensis may make it more susceptible to mortality or removal by scouring of sediments (Roegner et al., 1995). Another possible control on P. amurensis densities is predation by benthic predators, which also depends on prey burial depth and size (Richman and Lovvorn, 2003, in press, and references therein). Potamocorbula amurensis was the main prey of Lesser Scaup during the winters of 1998e99 and 1999e2000 (J. Y. Takekawa, unpubl. data), and of white sturgeon (Accipenser transmontanus) in nearby Suisun Bay in spring 1989 (Urquhart and Regalado, 1991). In contrast to P. amurensis, there were only minor declines in M. balthica densities between fall 1999 and spring 2000 although M. balthica is less tolerant of low salinity. Thus, sediment movement and predation by scaup, rather than decreased salinity, may have contributed to overwinter declines in P. amurensis. 4.2. Absence of Gemma and Ampelisca Two organisms were notably absent from our samples: with a 1-mm sieve, we found no Gemma gemma clams or Ampelisca abdita amphipods which were common in earlier studies (Nichols and Thompson, 1985b), although we found many empty G. gemma valves. Nichols and Thompson (1985b) noted that even

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a) Potamocorbula amurensis Lag = 1 m

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Lag distance (m) Fig. 6. (aec) Correlograms for the three most common benthic bivalves at six sites in San Pablo Bay (Fig. 1), 19 Octobere17 December 1999. Standard errors are not shown as they are mostly too small to be visible. Solid circles are different from 0 (z-test with Bonferroni adjustment, experimentwise a!0:05 for all tests combined within site and scale).

common species sometimes become scarce in San Francisco Bay, especially in response to high freshwater inflows. Gemma gemma requires salinities above 10 (Castagna and Chanley, 1973), and A. abdita is said not to tolerate low salinities (Nichols and Pamatmat, 1988; Nichols and Thompson, 1985a) although exact values were not given. In the winters of 1996e1997 and 1997e1998, strong El Nin˜o-Southern Oscillation events caused heavy precipitation and extremely high freshwater inflows (Fig. 7). Freshwater inflows above the 40-year mean also occurred early in 1999 and 2000, when big storms caused salinity in San Pablo Bay to fall from 19 to 4.5 between 11 and 28 February 2000 (N. Knowles, Scripps Institution of Oceanography, La Jolla, California 92037, pers. comm., Fig. 7). Gemma gemma requires salinities from 10 to 30 for reproduction (Castagna and Chanley, 1973), but such relatively high salinities would not be

maintained in San Pablo Bay during wet winters as in 1997e2000. Consecutive wet winters might prevent establishment of several year classes, necessitating transport of adults or juveniles from elsewhere for recolonization (Mills, 1967; Thompson, 1982; Commito et al., 1995a,b; Cummings et al., 1995). Recolonization by G. gemma and Ampelisca abdita might be further impeded by the more persistent, euryhaline Potamocorbula amurensis. Even in the South Bay where floodwater inflows are only a small fraction of those entering San Pablo Bay, it took about two years for A. abdita to recolonize after a high-inflow El Nin˜o year in 1982 (Nichols and Thompson, 1985a). 4.3. Effects of sediments Sediment particle size and organic matter content differed between sites, probably due to bathymetry and

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wind-driven waves resuspend smaller particles and redeposit them in deep channels (Sustar, 1982). Finer sediments are generally found in late fall and winter when wind-driven circulation is weak and freshwater inflows bring more fine sediments into San Pablo Bay. We may have sampled sediments too late in the fall to detect the coarse sediment pattern of summer, so that the settled small particles of our fall samples were similar to those found later in winter that are associated with high freshwater inflows. In at least some of our study periods, Potamocorbula amurensis and Macoma balthica were positively associated with finer sediments and lower organic matter, while Mya arenaria was associated with coarser particles and higher organic matter. Finer sediments generally adsorb more organic matter (a pattern not observed in our study) and provide more surface area for microbial attachment (Thomson-Becker and Luoma, 1985); however, fine sediments can also become depleted of oxygen. Tidal variations and hydrodynamic effects not measured in this study may have confounded relations between clam densities and sediments, causing effects to be detectable in M. balthica only in the spring and in M. arenaria only in the fall. For M. balthica, such factors vary widely in degree and direction of correlation in different studies (reviewed in Azouzi et al., 2002). We did not measure changes in sediment elevation, but we suspect sediment erosion may often scour benthic invertebrates in San Pablo Bay (Emerson and Grant, 1991). Burial by shifting sediments may also occur, although many shallow siphonate feeders such as Macoma balthica and Potamocorbula amurensis can escape burial quite well (Kranz, 1973). Faunally depauperate areas may be recolonized by adults and juveniles that are scoured and transported from

c) Mya arenaria Lag = 100 m

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exposure to currents and waves (Sustar, 1982). However, neither particle size nor organic matter content differed between seasons at the same sites. Other investigators have shown that sediment particle size in San Francisco Bay varies seasonally, with coarser sediments occurring in late spring and summer when

250,000 200,000 150,000 100,000 50,000 0 30 20 10 0

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Date Fig. 7. Mean monthly inflow in cubic feet per second (cfs) from the Sacramento/San Joaquin rivers into northern San Francisco Bay (Zdelta outflow, top) and concurrent mean salinity from the center of San Pablo Bay (bottom) from October 1997 to April 2000. The dashed line is mean inflow from 1956e1996. Delta outflow data are from the California Department of Water Resources Interagency Ecological Program (I.E.P.) website, http://iep.water.ca.gov. Salinity data are from N. Knowles, pers. comm.

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elsewhere in the bay or from coastal areas via the Golden Gate Channel (Mills, 1967; Thompson, 1982; Commito et al., 1995a,b; Cummings et al., 1995). We could not access the Bel Marin site in spring because sediment deposition made the water too shallow for our 5-m boat. In a previous study in the South Bay, sediment elevation decreased by 8 cm in one month, and was then restored completely in another two months (Nichols and Thompson, 1985b). Because water flows and sediment inputs are higher in San Pablo Bay, rates of erosion and deposition may be greater than in the South Bay. 4.4. Recruitment patterns Very low clam densities in spring samples obscured clear patterns of recruitment and growth. However, Potamocorbula amurensis spawned between November and April as shown by appearance of a smaller size class in the spring samples at Castro Cove and perhaps at Mare Island and China Camp (although only two small clams were found at China Camp). This recruitment highlights the ability of P. amurensis to reproduce at very low salinities (Nicolini and Penry, 2000). Potamocorbula amurensis in San Pablo Bay did not seem to spawn at the same time as conspecifics in Korea, which spawned twice a year during MayeJuly and SeptembereOctober (Lee, 1999). Macoma balthica was expected to show a new size class in spring samples, as this clam spawns between January and March in San Francisco Bay and grows rapidly (3.7 mm mo
1) after February (Nichols and Thompson, 1982; Thompson and Nichols, 1988). We found only a few new M. balthica at Mare Island, indicating that recruitment by M. balthica may have failed in spring 2000. However, if spawning was delayed until March and April in 2000, newly settled clams might have been too small to be retained by our 1-mm sieve. Macoma balthica can have reproductive failure during years when water temperature stays relatively warm or when salinity is low (Nichols and Thompson, 1982; Thompson and Nichols, 1988; Honkoop and Beukema, 1997). Mya arenaria in San Francisco Bay spawns between April and October with a peak in May and June (Rosenblum and Niesen, 1985). As expected, we found no new M. arenaria in spring samples which were collected in March and early April. 4.5. Dispersion and patch size In this study, Moran’s I based on spatial autocorrelation was more sensitive to variations in invertebrate density than Green’s Index of dispersion (GI) based on variance:mean ratios. GI values indicated that the clams exhibited slightly clumped to mostly random dispersion. However, the term ‘‘clumped’’ in reference to GIdor

469

any other dispersion index based on variance:mean ratiosdsays nothing about spatial associations among samples; i.e., ‘‘clumped’’ does not mean that locations with high invertebrate density tend to occur near other locations with high density. Rather, ‘‘clumped’’ in this case means only that invertebrates occur in higher densities in some samples than others, and no dependence on densities of neighboring locations is implied. In fact, parametric means and variances used in the formula for GI assume that all samples are independent and not spatially correlated. If all samples tend to have about the same density, then variance will be low relative to the mean and GI will be negative (‘‘uniform’’); if samples with a wide range of densities all occur with similar frequency, variance will be high relative to the mean and GI will be positive (‘‘clumped’’). Thus, inference based on GI that the frequency distributions of major macroinvertebrates were mostly random does not preclude strong patch structure. In contrast, correlograms created with Moran’s I illustrate spatial associations among samples. Because parametric means and variances assume that all samples are independent and that samples at different distances apart are not correlated, one should consider patch structure in the spacing of samples to be used in parametric statistics (e.g., transect means and tests between them). Positive values of Moran’s I indicate that samples at given distances apart are similar, whereas negative values indicate dissimilarity. Moran’s I also provided information about patch structure through interpretation of correlograms (Sokal, 1979; Legendre and Fortin, 1989). Different data collection methods affect the shape of correlograms, so comparisons between this study and others must remain qualitative. However, our results revealed some patterns and variations among bivalve species and study locations. Small-scale patch size for all three clam species varied among sites around San Pablo Bay, ranging from 1 m (the finest resolution of this study) to 5 m or greater (we do not know if spatial autocorrelation occurred between 5 and 100 m). Potamocorbula amurensis showed significant autocorrelation at around 100 m at all sites, as did Macoma balthica and Mya arenaria at most sites. This pattern suggests repetitive occurrence of patches at about 100 m. Potamocorbula amurensis also showed this pattern at 900e1000 m at three of six sites, indicating that P. amurensis patches may occur at a range of spatial scales. At three or more sites in our study, M. balthica densities showed decreasing similarity with increasing distance. In the South Bay, Thompson (1999) sampled with a van Veen grab in a systematic pattern on a 20!20 m grid. Her analyses revealed no significant autocorrelation for any bivalve species except Potamocorbula amurensis, although autocorrelation for the other species might not have been detected owing to their low densities. As in our

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study, P. amurensis in the South Bay also occurred in small patches nested within larger patches, although the smallest patch size was !1 m for three out of four sites studied (Thompson, 1999). Thompson (1999) suggested that the patch structure she found was influenced by phytoplankton availability to P. amurensis as water flowed over patches of different sizes. In our study, no strong spatial patterns occurred at any one site for all three bivalve species. The most abundant clams generally showed the strongest patterns, but this may be an artifact of the spatial autocorrelation technique which is influenced by the number of individuals (Gage and Geekie, 1973). Large-scale bivalve dispersion seemed to follow species-specific patterns at some but not all locations, a phenomenon also observed by Schneider (1987). There were also species-specific differences in variability within nesting level in the nested ANOVA; in particular, Macoma balthica exhibited little variation on the scale of meters, whereas Potamocorbula amurensis and Mya arenaria showed significant variation at that scale. Differences in siphon length, the ability of M. balthica to deposit-feed, and differential response to water flow, food supply, sediment scouring, predation, or other effects may have contributed to these different patterns. We did not sample sediments in a way that allowed comparison of invertebrate patch structure to sediment characteristics, but patterns of species density may have been affected by sediments (Tenore et al., 1968; Vincent et al., 1994). When spatial autocorrelation is used together with a mean:variance dispersion indicator such as Green’s Index, one can also infer the ecological processes responsible for the observed patterns. According to Sokal (1979), it is unlikely to observe, as we did, random dispersion according to Green’s Index along with significant autocorrelation. This combination of indices suggests random distribution of settling recruits, followed by nonrandom mortality or dispersal (Sokal, 1979). Such a pattern does not seem so unlikely in this shallow estuary if wind-driven circulation moves larvae in a stochastic manner, but post-settlement mortality or redistribution is patchy according to food availability, density-dependent factors or predation (Luckenbach, 1984; Thrush et al., 1994; Commito et al., 1995b; Whitlatch et al., 1997; Thompson, 1999). 4.6. Conclusions San Pablo Bay is an important habitat for benthic predators like diving ducks, sturgeon, flatfish, sharks, rays and crabs. However, as in many other arid and semiarid estuaries, naturally wide variations in freshwater inflow have been magnified by major water diversions (Cayan and Peterson, 1993; Longley, 1994; Baird and Heymans, 1996; Schumann and Pearce, 1997; Rodriguez et al., 2001). Such changes, along with exotic invasions

that are often facilitated and maintained by changes in freshwater inflow, can have important effects on prey availability. Moreover, diving ducks and sturgeon in northern San Francisco Bay have been found to have elevated levels of selenium and heavy metals in their tissues (Ohlendorf et al., 1986; Urquhart and Regalado, 1991; Miles and Ohlendorf, 1993), and Macoma balthica and Potamocorbula amurensis are being considered as biosentinel species for selenium and metal contamination. Potamocorbula amurensis appears to be a more sensitive indicator, as it acquires selenium, cadmium, chromium and zinc at a higher rate than M. balthica (Brown and Luoma, 1995; Lee et al., 1998; Linville et al., 2002). Contamination of P. amurensis by selenium is spatially and temporally variable (Linville et al., 2002), thereby increasing complexity in relations between freshwater inflow, spatial and temporal dispersion of prey, and bioaccumulation. Climate warming, increased diversion of water for human use, and invasions by exotic species will likely increase the impacts of reduced and variable freshwater inflow on the biota of semiarid estuaries. When monitoring benthic prey availability or potential contaminant uptake by mobile benthivores in areas such as San Pablo Bay, sampling programs should account for wide variations in benthic macroinvertebrate densities. Sampling should be done at multiple locations with multiple samples at each location. Samples at a given site should be at least 5 m apart to achieve sample independence and to account for between-patch variation in bivalve abundance. Temporal variation in invertebrate populations over winter is also very high, so researchers must take multiple samples over time to assess prey availability and potential contaminant exposure for wintering waterfowl or benthivorous fish. Acknowledgements This work was funded by the Coastal Program of the U.S. Geological Survey. We appreciate the help of A. K. Miles, K. J. Phillips, S. E. Wainwright-De La Cruz, J. L. Yee and staff at the San Francisco Bay Estuary Field Station of the U.S. Geological Survey. Field work would not have been possible without the excellent assistance of N.A. Farnau and the further help of M.W. Poulton. D.E. Legg and K.G. Gerow gave advice on statistical approaches, and J.S. Meyer provided guidance on sediment analysis. N. Knowles generously provided salinity data and his website was especially helpful.

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