Biological Invasions 3: 23–36, 2001. © 2001 Kluwer Academic Publishers. Printed in the Netherlands.
Assessing invader roles within changing ecosystems: historical and experimental perspectives on an exotic mussel in an urbanized lagoon Jeffrey A. Crooks Scripps Institution of Oceanography, University of California, San Diego, 0218, La Jolla, CA 92093-0218, USA; Present address: Smithsonian Environmental Research Center & Romberg Tiburon Center, 3152 Paradise Drive, Tiburon, CA 94920, USA (e-mail:
[email protected]; fax: +1-978-428-2661) Received 4 April 2000; accepted in revised form 1 May 2001
Key words: Bivalvia, Chione fluctifraga, Chione undatella, competition, ecosystem engineering, Macoma nasuta, Musculista senhousia, sliding baselines, Solen rostriformis Abstract It is often difficult to accurately assess the long-term effects of invaders because of a lack of data and the changing nature of ecosystems. However, available historical information can be used to make comparisons with current conditions and generate hypotheses that can be tested experimentally. This approach was used to examine changes in the bivalve community of Mission Bay, San Diego, California, USA. A 20-year dataset on subtidal bivalves shows a marked increase in abundance of the exotic mussel Musculista senhousia, and concomitant declines in species richness and the abundance of the native Solen rostriformis. Currently, Musculista also dominates the tidal creeks of a remnant salt marsh and an adjacent restored marsh, and is 100 times more abundant than any native bivalve species. A comparison of the bivalves now present in the remnant marsh creek to the community present 35 years ago demonstrates that while Musculista increased in abundance, the native Chione fluctifraga disappeared from the creek. In the same time frame, two other natives, Macoma nasuta and C. undatella, appeared in the system. Experiments demonstrate that the growth and survivorship of the surface-dwelling, suspension-feeding Chione spp. significantly decrease in the presence of Musculista, whereas the deeper-dwelling, deposit-feeding Macoma nasuta shows no such inhibition. Viewing these results in the broader context of physical change within the wetland explains some patterns of observed change and suggests effects due at least in part to Musculista, but also demonstrates the complexities associated with assessing long-term patterns in systems affected by multiple factors. Introduction A continuing challenge in assessing the role of alien species is determining their long-term impact (Parker et al. 1999; Ruiz et al. 1999). Because invasions of exotics and the onset of their impacts often predate thorough biological investigations of recipient ecosystems, ecological responses to invasions may go unnoticed (Carlton 1996; Ruiz et al. 1997). Invader effects also may be confounded by biotic responses to other potentially interrelated changes in ecosystems, including habitat destruction, pollution, and resource over-exploitation (Ruiz et al. 1997; Mooney and Hobbs 2000). In order to address the long-term
effects of invasions and other anthropogenic activities within these changing ecosystems, it is necessary to obtain historical perspectives. Although pre-impact information is typically scarce, available qualitative or quantitative historical data, even if for already impacted systems, can be beneficial (Droege et al. 1998; Rackham 1998; Shaffer et al. 1998). Such data can be utilized to offer insight into how and why ecosystems have changed (e.g. Steedman et al. 1996; Patton et al. 1998) and establish benchmarks for conservation and restoration efforts (Dayton 1998; Dayton et al. 1998). Historical information also can be viewed in conjunction with results from short-term manipulative experiments to further understand effects of invaders
24 against a backdrop of historical change (Byers 1999, 2000). Nearshore marine ecosystems, including bays, estuaries, and lagoons, are often heavily impacted by anthropogenic activities, including the intentional and unintentional introduction of exotic species (Norse 1993; McNeely et al. 1995; Ruiz et al. 2000). Although many alterations in these systems remain undocumented (Dayton et al. 1998), information on target taxa can highlight broad patterns of change. In these aquatic habitats, bivalves provide a good basis for historical comparisons as they are common, often collected by naturalists, and well suited for assessing causal mechanisms of change because of their amenability to experimental manipulation (e.g. Peterson 1977; Ricciardi et al. 1997; Crooks and Khim 1999). In addition, bivalves themselves can be important agents of change when introduced into ecosystems (Carlton 1992; Strayer 1999; Strayer et al. 1999). Clams and mussels such as Dreissena spp. and Corbicula spp. in freshwaters (Phelps 1994; Morton 1997) and the Asian clam Potamocorbula amurensis in San Francisco Bay (Alpine and Cloern 1992; Kimmerer et al. 1994) are well known for their system-wide ecological effects. In southern California soft-sediment habitats, an exotic, mat-forming mussel, Musculista senhousia, has become a dominant invader that has dramatic effects on small macrofauna and eelgrass (Crooks 1998a,b; Reusch and Williams 1998; Crooks and Khim 1999). In this region, the dense byssal mats created by this mytilid mussel represent a novel life habit, as no other bivalves create these biogenic structures. To address long-term changes in a bivalve community and highlight the role of M. senhousia (hereafter referred to as Musculista) within an urbanized marine ecosystem, a study was conducted in Mission Bay, San Diego, California, USA (Figure 1). Over the last 150 years, Mission Bay has been heavily modified, including diversions of its principal source of freshwater input, organic enrichment and other pollution, wetland loss, dredging, filling, and dumping of sand on beaches (Chapman 1963; Marcus 1989; Herring 1991; Dexter and Crooks 2000). Following these major alterations, a small remnant (30 ha) salt marsh and mudflat remained in the northeast corner of the bay (the Northern Wildlife Preserve and Kendall Frost Reserve). In December 1995, a 2.8 ha plot of filled land adjacent to this remnant salt marsh, the Crown Point Mitigation Site, was returned to intertidal depths for the creation of new salt marsh and tidal creek habitats (Figure 1D).
Qualitative records from Mission Bay offer a general benchmark for the bivalve communities that existed around the turn of the 20th century (Orcutt and Dall 1885; Hemphill 1891; Kelsey 1907; Weymouth 1921; Morrison 1930). The bay’s tidal flats and salt marshes supported a rich bivalve fauna consisting of several large species, including the sunset clam Gari californica, the California butterclam Saxidomus nuttalli, the flat clam Semele decisa, and the gaper clam Tresus nuttallii. These species are now uncommon or absent in the intertidal, probably resulting from a combination of habitat destruction and over-harvesting (Morrison 1952a,b, 1954, 1957; Chapman 1963). Some of the clams present today (Hertz and Hertz 1992; S. Rugh pers. comm.; Crooks pers. obs.) that were also common historically include the cockles Chione undatella and C. fluctifraga, the littleneck clam Protothaca staminea, the scallop Argopecten ventricosus, the jackknife clam Tagelus californianus, and the bent-nosed clam Macoma nasuta. Among the most conspicuous changes to the bivalve assemblage in the bay have been the invasion of exotic species. Two exotic bivalves, Musculista (Crooks 1992, 1998a) and the Mediterranean blue mussel Mytilus galloprovincialis (Suchanek et al. 1997; Crooks, pers. obs.) are now abundant in the bay. Two quantitative historical datasets on bivalves in the bay are available: a time-series sampling in the subtidal since 1977 (Dexter and Crooks 2000; Dexter, unpub. data), and a study of salt marsh mollusc fauna in the mid-1960s (MacDonald 1967, 1969a,b). In this paper, I will use these data as well as additional sampling and experimentation to: (1) assess temporal trends in the subtidal bivalve community, (2) compare the bivalve community of the salt marsh tidal creek in the mid-1960s and mid-1990s, (3) test experimentally the hypothesis that the effects of Musculista on some dominant bivalves are consistent with observed longterm population trends of these species, and (4) examine the bivalve colonization of a newly-created tidal creek.
Materials and methods Subtidal bivalve sampling Quantitative subtidal data from Mission Bay were collected in conjunction with the Biological Oceanography class at San Diego State University (Dexter 1983;
25
Figure 1. Mission Bay, San Diego, California (32◦ 47 N, 117◦ 14 W). (A) Spanish map from 1782 (adapted from Pourade 1960), showing Mission Bay with extensive wetlands. (B) The bay as it appeared in 1931 (adapted from Chapman 1963). Note the location of the San Diego River, which was diverted into Mission Bay in the 1850s, causing much of the south bay to fill with sediment. (C) Mission Bay as it appears now, after the post-World War II dredging, filling, and San Diego River diversion operations (adapted from Dexter 1983). Letters represent the location of the subtidal stations. (D) Close-up of the Northern Wildlife Preserve and Crown Point Mitigation Site, showing the two natural creeks (Creeks 1 and 2) and the restored creek. MLLW = Mean lower low water.
Dexter and Crooks 2000). From 1977 to 1996, seven back-bay stations were sampled using a conical orangepeel grab (surface area = ca. 0.1 m2 ; depth = ca. 15 cm; average volume = 4.5 l) deployed from a boat. Five of these stations will be considered in this paper (Figure 1C). Water depth at the stations was 4–5 m, and four to seven replicate grabs were taken at each station on each sampling date. Samples were sieved through a 750-µm mesh and sorted under a dissecting microscope. The data from these samples were used to investigate temporal patterns of abundance of two dominant species, the Japanese mussel Musculista and the razor
clam Solen rostriformis (= S. rosaceus), as well as patterns in bivalve species richness. Regression analyses were used to assess temporal trends in these species. Tidal creek bivalve sampling Quantitative sampling of the tidal creek bivalve community at the Northern Wildlife Preserve was conducted using the sampling methods described by MacDonald (1967, 1969a,b), in his studies of the same creek (Creek 1, Figure 1D). Thus, direct comparisons of the composition and abundances of the bivalve
26 community were possible (although only means were reported in the 1960s study, so no statistical tests were carried out). In 1965 and 1966, 10–33 samples were taken in the creek on each of five dates (MacDonald 1967). Between 1994 and 1996, 10–12 samples were taken on each of four dates. In addition, on one date sampling was done on nearby natural and restored creeks (Figure 1D) using the same methodology. In April 1994, six stations were sampled, each containing a pair of adjacent quadrats (the paired sampling in MacDonald (1967)). The average value of the quadrats was used for calculation of mean abundances. On all other dates (September 1994, July 1995, and December 1996), only one quadrat at each of 10 stations was sampled. As in the 1960s study, stations were spaced at approximately equal intervals along the length of the tidal creek. In December 1996, 12 additional stations were sampled: 9 in the 11-month-old tidal creek (Crown Point Mitigation Site, Figure 1D), and three in the short, adjacent natural creek (Creek 2, Figure 1D). Stations were stratified approximately equidistantly along the creek. Sampling consisted of excavating sediment from a surface area of 0.0625 m2 to a depth of approximately 25 cm. This depth was determined to be sufficient to adequately sample all but the deepest burrowing bivalves (e.g., T. californianus and Cryptomya californica) (MacDonald 1967). Samples were sieved in the field through 1mm mesh and all material retained was preserved in buffered formalin (MacDonald 1967). Bivalves were sorted in the laboratory under a dissecting microscope and identified to species or the lowest taxonomic level possible (Keen and Coan 1974; McLean 1978; Morris et al. 1980; Reish 1995; Coan et al. 2000). For all samples, Musculista shell lengths were also measured, and the length-weight regressions in Crooks (1996) were used to estimate mussel biomass. Statistical differences in Musculista densities and biomass in the restored and natural creeks were assessed using t-tests assuming unequal variance (Microsoft Excel© ). Manipulative experiments Two experiments were conducted that tested whether direct interactions between Musculista and three native clam species were consistent with the long-term trends observed in the system. These experiments examined the growth and survivorship of M. nasuta, Chione undatella, and C. fluctifraga, all of which exhibited
changes in abundance over the last thirty years, but are still present in some locations within Mission Bay. The experiments were conducted on the unvegetated tidal flat in the Northern Wildlife Preserve adjacent to the tidal creek, at a tidal elevation of approximately 0.25 m above Mean Lower Low Water. This site was chosen because of its suitability for the experimental layout and to minimize disturbance in the protected marsh habitat. Experiment 1 – Musculista senhousia versus Macoma nasuta In this experiment, growth and survivorship of the deposit-feeding clam, Macoma nasuta, were assessed in the presence and absence of Musculista. The experiment was arranged as a Randomized Complete Block design with 12 blocks of two cages each. The experimental units were topless mesh (1.4 mm) enclosures (10 cm in diameter and 14 cm deep) that received one of two treatments: (1) three M. nasuta with Musculista and mats in ambient densities (approx. 60 mussels per enclosure ), or (2) three M. nasuta without mussels and mats. At the beginning of the experiment, clams and mussels were collected from the muddy intertidal flats of east Mission Bay near Tecolote Creek (Figure 1). Prior to the experiment, clams were immersed in a bath of Calcein (a phosphorescent, calcium-binding tag often used for assessing growth) for 24 h (Rowley and MacKinnon 1995). At the experimental site in the Northern Wildlife Preserve, holes were excavated to a depth of approximately 12 cm, which allowed ample burrowing depth for this species. Enclosures were placed in the sediment with approx. 2 cm of projecting fence edge. The enclosures were then filled with the natural, unsieved sediment (which contained no detectable bivalves) removed from the plot. The enclosures within a block were approximately 1 m apart. After cage installation, three M. nasuta were placed in each cage (representing densities lower than those encountered at the collection site). Clams of a small size range were chosen to minimize potential effects of initial size on percent growth. The average initial lengths (±1 s.e.) of M. nasuta in the treatment and control plots were respectively 7.0 ± 0.4 and 6.9 ± 0.2 mm. After allowing sufficient time for clam burial (one day), one randomly selected cage in each block received the mussel treatment. To best represent natural conditions, mussels in their unaltered byssal mats, containing sediments, detritus, small
27 organisms, and algae, were placed on the sediment surface in one enclosure in each of the 12 blocks. Each enclosure was then covered with a sideless cage (0.5 m tall) with coarse vinyl mesh (2.5 cm) on top to prevent shorebird predation on the transplanted mats (which are more vulnerable than larger, natural mats; see also Crooks and Khim 1999). Effectiveness of cages was judged by visual observation of bird feeding behavior and lack of bird foot prints and ripped-up mats in cagecovered plots. The experiment began in December 1996 and ran until June 1997. During the course of the experiment, enclosures were occasionally cleared of algae and, in the control enclosures, of obvious clumps of naturally recruiting mussels. At the end of the experiment, all contents of the cages were sieved through 1-mm mesh. The response variables in the experiment were percent survivorship and percent growth of M. nasuta. Survivorship was determined as the number of clams found alive (out of the original three) in each enclosure at the end of the experiment. Percent growth was to be measured using the Calcein tag. However, in addition to tagging the shell, the Calcein produced a narrow discolored band that was also visible with the naked eye. Initial clam size was measured from the umbo to this growth check, and growth was the distance from the check to the ventral margin of the shell. Randomized Complete Block ANOVAs were used to test for statistical differences in survivorship and growth in the two treatments. To examine potential effects of mussels on clam soft-tissue growth, lengthweight relationships (for one clam from each enclosure) were also examined. Sub-samples of the mussels were counted and their shell lengths measured to estimate mussel biomass. Experiment 2 – Musculista senhousia versus Chione undatella and Chione fluctifraga In this experiment, growth and survivorship of the two shallow-dwelling, suspension-feeding clams, C. undatella and C. fluctifraga, were measured in the presence and absence of Musculista in its mats. The experiment was arranged as a Randomized Complete Block design, with 18 blocks for C. undatella and 18 for C. fluctifraga. The experimental units were topless mesh (1 cm) enclosures (10-cm in diameter and 8-cm deep) that received one of two treatments: (1) one clam and mussels in their mats in ambient densities (approx. 40 mussels per enclosure), or (2) one clam
and no mussels. The average initial lengths (±1 s.e.) of the C. undatella in the treatment and control plots were respectively 17.5 ± 0.8 and 17.1 ± 0.7 mm. For C. fluctifraga, average initial lengths in the treatment and control plots were respectively 17.1 ± 0.6 and 17.3 ± 0.5 mm. At the experimental site, holes were excavated to a depth of approximately 6 cm, and enclosures placed in the sediment with approx. 2 cm of projecting fence edge. The enclosures were then filled with the natural, unsieved sediment removed from the plot. The enclosures within a block were approx. 0.5 m apart. The blocks were again covered with sideless mesh enclosures (0.5 m high, 2.5 cm mesh) to prevent shorebirds from preying upon mussels. During the course of the experiment, which ran from August to December 1997, plots were occasionally cleared of macroalgae and mussel clumps removed from control enclosures. At the conclusion of the experiment, clams were collected for assessment of survivorship and growth. Survivorship was determined as the number of clams found alive at the end of the experiment, divided by the total number of live plus dead clams found at the end of the experiment. Experimental units in which neither dead nor live clams could be found (total of four) were excluded from the analysis. Clam length (from the posterior to the anterior margin of the shell) was measured with digital calipers prior to the experiment. Clams found alive at the end of the experiment were again measured, and growth (if any) was the change in length. Fisher’s exact tests were conducted to detect statistical differences in mortality. Percent growth in clams surviving the duration of the experiment was examined using t-tests assuming unequal variance. The experiment was not analyzed as a Randomized Complete Block ANOVA because of a strong treatment effect which left few clams in the presence of mussels alive at the end of the experiment (see Results). Samples of mussels in the treatment and control enclosures were counted and measured for shell length, and biomass in the plots estimated.
Results Subtidal bivalve communities Sampling in the subtidal sediments of Mission Bay from 1977 to 1996 revealed the presence of 17 bivalve
28 Table 1. Bivalve species found in the quantitative subtidal and salt marsh creek samples. Species Cardiidae Laevicardium substriatum Lyonsiidae Lyonsia californica Mactridae Mactrotoma californica Myacidae Cryptomya californica Mytilidae Musculista senhousia∗ Mytilus galloprovincialis∗
Petricolidae Cooperella subdiaphana Pholadidae Unidentified juvenile Semelidae Theora lubrica∗ Solecurtidae Tagelus californianus Solenidae Solen rostriformis Tellinidae Macoma nasuta Macoma sp. Tellina sp. Veneridae Chione californiensis Chione fluctifraga Chione undatella Protothaca staminea Unidentified
Common name
Subtidal Creek
Egg-shell cockle
x
California lyonsia
x
California dish clam
x
California softshell
x
x
Japanese mussel, cuckoo mussel Blue mussel, bay mussel, Mediterranean mussel
x
x
x
x
Shiny cooperclam
x
Piddock
x
Asian semele
x
California jack-knife clam
x
Rosy razor clam
x
Bent-nosed clam Tellin California cockle Smooth cockle Wavy cockle Pacific littleneck
x
x x x x x x x x
x x x
Figure 2. Historical trends in subtidal bivalve populations in Mission Bay. (A) Densities of the exotic mussel, Musculista senhousia. (B) Densities of the native razor clam Solen rostriformis. (C) Total densities and numbers of species for all other bivalves combined (excluding M. senhousia and S. rostriformis).
early years of the study, has declined in abundance (F1,14 = 8.98, P = 0.010). The total density of the other bivalves varied over the course of the study but remained relatively low and showed no temporal trends (F1,14 = 0.02, P = 0.894). The number of species of other bivalves, however, has declined over the sampling period (F1,14 = 5.04, P = 0.041). Tidal creek bivalve communities
∗ Exotic.
species (Table 1). The most dramatic trend in these subtidal populations has been the increasing abundance of the introduced mussel Musculista (Figure 2). This species has significantly increased in abundance over the two decades in which the populations have been monitored (F1,14 = 27.61, P < 0.001). Over the same time period, the razor clam, S. rostriformis, which was one of the most abundant clams in the
In total, seven bivalve species were found in the quantitative natural creek samples of the Northern Wildlife Preserve (Tables 1 and 2). Sampling revealed a total of five species in the 1990s, and five in the 1960s (Table 2). Only three of the seven species, Musculista, T. californianus, and P. staminea, were found at both times. Macoma nasuta was found in the 1990s, but not in 1960s (although M. nasuta shells were found in the earlier sampling). Chione undatella also appeared in the tidal creek in the 1990s, represented by one
29 Table 2. Average (A) bivalve densities (±1 s.e.) and (B) estimated Musculista biomass (±1 s.e.) in Creek 1 (Figure 1D) on each sampling date during the 1990s, and averages across all dates for the 1990s and 1960s.a 1994–1996
(A) Bivalve densities
1965–1966 Average
April 1994
September 1994
July 1995
December 1996
Average
154.7 (±30.5) 1.3 (±1.3) 0 0 1.3 (±1.3) 4.0 (±1.8) 0 161.3 (±32.2)
380.8 (±112.6) 4.8 (±2.4) 0 0 0 8.0 (±2.7) 0 393.6 (±113.0)
2038.4 (±681.8) 17.6 (±6.1) 1.6 (±1.6) 0 0 1.6 (±1.6) 0 2059.2 (±684.2)
188.8 (±49.7) 0 0 0 0 1.6 (±1.6) 0 190.4 (±49.0)
690.7 (±452.0) 5.9 (±4.0) 0.4 (±0.4) 0 0.3 (±0.3) 3.8 (±1.5) 0 701.1 (±455.6)
0.70 (±0.17)
9.07 (±3.38)
(m−2 )
Musculista senhousia Macoma nasuta Chione undatella Chione fluctifraga Protothaca staminea Tagelus californianus Cryptomya californica Total
7 0 0 7 3 2 1 20
(B) Musculista Biomass (g dfw∗ m−2 ) 0.15 (±0.03)
1.37 (±0.86)
2.82 (±2.10)
0.02
a From
MacDonald (1967). dfw = dry flesh weight.
individual in the quantitative samples (although it was also occasionally observed in qualitative sampling). Cryptomya californica and Chione fluctifraga were absent from quantitative (as well as qualitative) creek samples in the 1990s. During the 30 years between the two sampling periods there were dramatic changes in bivalve abundances and biomass (Table 2). The total density of bivalves in the system increased from an average of 20 individuals per m2 in the 1960s to over 700 individuals per m2 in the 1990s. Of the species in common between both dates, T. californianus on average remained in approximately comparable densities, and P . staminea experienced about a 10-fold decrease in abundance (with only one individual found in the 1990s’ quantitative samples). Musculista showed a very large change, increasing in abundance and biomass by about two orders of magnitude (Table 2). This exotic mussel, which was first collected in Mission Bay in the 1960s sampling (MacDonald 1967), went from comprising about 33% of the total number of bivalves to 99% of the total thirty years later. Whereas Musculista were found singly in the 1960s (MacDonald 1967), in the 1990s they were typically found aggregated in byssal mats, with a maximum density at a station of over 5500 mussels per m2 and a maximum biomass of over 23 g dfw (dry flesh weight) per m2 . Quantitative sampling in the tidal creek of the newly created marsh (the Crown Point Mitigation Site) revealed the presence of four bivalve taxa (Table 3). Musculista was the most abundant species. Its density in the restored creek was about five times higher
Table 3. Average (A) bivalve densities (±1 s.e.) and (B) estimated Musculista biomass (±1 s.e.) in the two natural creeks and the 11-month old restored creek (Figure 1D) in December 1996. Creek 1
Creek 2
Restored creek
Mytilus galloprovincialis
188.8 (±49.7) 0
144.0 (±72.1) 0
Macoma nasuta
0
Protothaca staminea
0
5.3 (±5.3) 0
901.3 (±428.7) 3.6 (±3.6) 0
Tagelus californianus
1.6 (±1.6) 0
0
190.4 (±49.0)
149.3 (±69.9)
1.8 (±1.8) 908.4 (±430.0)
0.40 (±0.15)
14.00 (±10.77)
(A) Bivalve densities (m−2 ) Musculista senhousia
Pholadidae Total
0
1.8 (±1.8) 0
(B) Musculista Biomass (g dfw∗ m−2 ) 1.37 (±0.86)
than in both natural creeks (Table 3), although these differences were not statistically significant (t-tests; 0.15 > P > 0.10) due to large variances arising from spatial patchiness typical for this species (Crooks 1996). Mussel biomass was at least an order of magnitude higher in the restored creek (Table 3), although again this was not significant because of high variances (t-tests; 0.30 > P > 0.20). Maximum Musculista biomass at a restored creek station was over 99 g dfw
30 per m2 . Mytilus galloprovincialis, another exotic mussel, was the second most abundant species in the tidal creek (Table 3). Although its quantitatively-assessed densities were relatively low, this mussel was patchily distributed and had formed dense beds that did not occur at the sampling stations. Both Musculista and M. galloprovincialis grew rapidly in the creek. The largest Musculista collected in the quantitative samples was 24 mm. The largest M. galloprovincialis was 21 mm in the quantitative samples, and animals 51 mm in length were collected at the same time from other locations in the restored creek. Two juveniles of other species, a pholad and P. staminea, were also present in the restored creek (Table 3). In the natural creeks at the same time, Musculista, T. californianus, and Macoma nasuta were present (Table 3). Manipulative experiments In both experiments, the transplants of Musculista in their mats persisted well, with many live mussels and well-developed mats present at the conclusions of the experiments. In the M. nasuta experiment, the final density (mean ±1 s.e.) of mussels in the mussel treatment was 58.3 ± 6.6 per plot, and the average estimated total biomass was 1.9 ± 0.2 g dfw per plot. In control enclosures, final mussel density (mean ±1 s.e.) was 33.8 ± 4.5 per plot due to a recruitment event (in both treatment and control plots) near the end of the experiment and rapid growth of the mussel. However, these mussels were smaller (modal length of 14 mm compared to a modal length of 22 mm in the treatment plots), their average total biomass (±1 s.e.) was less than 1/3 that in the treatment plots (0.6 ± 0.1 g dfw per plot), they had not formed well-developed mats, and they were found primarily near the walls of the enclosures. Thus, their potential effect was considered small compared to that of the mussels in the plots containing dense, transplanted mats. In the Chione experiment, the average final densities (±1 s.e.) in the mussel transplant and control plots were 55.0 ± 6.6 and 2.0 ± 1.4 mussels per plot, respectively. The average total biomass (±1 s.e.) in the treatment and control plots were respectively 1.1 ± 0.1 and 0.02 ± 0.2 g dfw per plot. Macoma nasuta, which has increased in abundance along with Musculista in the remnant natural creeks (Table 2), was not significantly inhibited by the mussel. Average percent survivorship was relatively high (over 70%) in both the treatment and control, and no significant differences were found (Figure 3A). Similarly, no
significant differences in growth were found between the treatment and control (Figure 3B). Average final sizes (±1 s.e.) were 11.1 ± 0.2 and 11.7 ± 0.1 mm in the treatment and control plots, respectively. Also, no significant differences were found in the slopes of ln length/ln weight regression lines for clams with and without mussels (slope with mussels ±1 s.e. = 0.061 ± 0.023; without mussels = 0.073 ± 0.033). Unlike M. nasuta, C. undatella and C. fluctifraga were significantly inhibited by the presence of the mussel and its mats. Survivorship of these clams in the presence of mussel mats was less than 50% of that in plots without mats (Figure 3C). Of those clams surviving the duration of the experiment, growth in the mussel treatments was less than 25% of that in the control plots (Figure 3D). The average final sizes (±1 s.e.) of C. undatella in treatment and control plots were 18.3± 1.2 and 19.6±0.7 mm, respectively. Average final sizes of C. fluctifraga were 17.0 ± 0.6 and 19.5 ± 0.6 mm in the treatment and control, respectively.
Discussion The quantitative data spanning thirty years demonstrate that the bivalve communities of Mission Bay have undergone dramatic changes (Figure 2, Table 2). These include a population explosion of the exotic mussel Musculista which coincided with other shifts in extant bivalve communities. The experimental evaluation of Musculista effects on native clams suggests an important role of the invader in shaping some of these trends, although these must be viewed in the context of other changes in the system. Effects of Musculista on native clams The experiments demonstrate that Musculista negatively affects the survivorship and growth of the surface-dwelling, suspension-feeding clams C. undatella and C. fluctifraga (Figure 3). Although the ultimate cause of this inhibition is the presence of the mussels and its mats, there are a variety of proximate factors that might mediate these negative effects. Both competition for space and/or food, resulting from the activities of living mussels (e.g. filter feeding and biodeposition), and habitat modification likely play a role in the observed impact on clams. Because Musculista is a densely-living suspension feeder (Morton 1974; Crooks 1996), its filtration of
31
Figure 3. Results of experiments testing the effects of Musculista senhousia on the survivorship and growth of a deep-dwelling, deposit-feeding clam, Macoma nasuta (A and B), and two shallow-dwelling, suspension-feeding clams, Chione undatella and C. fluctifraga (C and D). P-values are from Randomized Complete Block ANOVA’s for % survivorship and growth for M. nasuta, Fisher’s exact tests for % survivorship of Chione spp., and t-tests for % growth of Chione spp. See text for more details.
near-bottom water may locally deplete food supplies (Allen 1999; Reusch and Williams 1999), thus affecting other clams (e.g. Peterson 1982). The mussel’s suspension feeding also might inhibit settlement of other bivalve larvae (e.g. Woodin 1976; Andr´e and Rosenberg 1991). However, other macrofaunal taxa with planktonic larval modes (e.g. annelids and gastropods) showed no negative relationship with mussels under both natural and experimental conditions (Crooks 1998b; Crooks and Khim 1999). Another
direct influence of living mussels may be biodeposition of feces and pseudofeces (mucus-bound material ejected from the siphon without passing through the gut). Sediments within and below well-developed mussel mats often have more organic matter, ammonium, and fine sediments than areas without mats (Crooks 1998b; Reusch and Williams 1998). This alteration of sediment properties, or the physical production of material that may interfere with the filtering ability of other clams, may inhibit other bivalves. In contrast,
32 Musculista, although a suspension-feeder, has adaptations for living in and processing fine sediments (Morton 1974). Musculista is an ecosystem engineer (sensu Jones et al. 1994, 1997) that modifies benthic habitats through its creation of structurally complex mats composed of shells, byssus, sediments, and detritus (Crooks and Khim 1999). Although the mat structure facilitates many small macrofaunal taxa, such as gastropods, crustaceans, polychaetes, and insect larvae (Creese et al. 1997; Crooks 1998; Crooks and Khim 1999), larger organisms not able to live within the mat matrix, such as clams, may be inhibited. As Musculista and Chione spp. both occupy the same, shallow depth horizon, the gregarious and fast-growing mussels may outcompete the solitary clams for space. Furthermore, it was observed in some experimental plots, and in natural settings, that Musculista can byssally attach to living clams. Although space is often not limiting in three-dimensional, soft-sediment environments (Peterson 1979, 1982, 1991; but see Peterson and Andr´e 1980), the mussel’s high densities and mat creation may limit living space for larger clams. Similarly, dense Musculista mats can inhibit the vegetative propagation of the native eelgrass Zostera marina (Reusch and Williams 1998). In contrast to the effects on Chione spp., Musculista had no significant effect on M. nasuta (Figure 3). This species typically lives deeper within the sediments, below mussel mats, and is primarily a deposit feeder with long siphons to feed on the sediment surface (Rae 1979). As M. nasuta growth was comparable (Figure 3) with and without dense mats, its feeding does not appear inhibited by the structurally complex mat (although laminar algal mats can inhibit Macoma nasuta; Everett 1994). Thus, this species may gain a refuge from the deleterious effects of Musculista in both feeding mode (i.e. deposit versus suspension) and burial depth. Relationship to long-term patterns The negative effects of Musculista on surface-dwelling, suspension-feeding cockles (Figure 3) provide a mechanism by which the mussel may have contributed to the order of magnitude decrease in native representatives of this guild of bivalves (C. fluctifraga and P. staminea) in the tidal creek (Table 2). Given that the fast-growing and abundant Musculista can cause mortality in the span of months (Figure 3), and because the native
clams have a longevity of at least two to three years (MacDonald 1967), it is possible that many individual clams would be exposed to potentially lethal conditions at some point in their lives. Results from short-term descriptive studies in other locations also have suggested a negative relationship between Musculista and other suspension-feeding bivalves, including Meretrix lusoria, Mactra chinensis, Mactra veneriformes, and Xenostrobus pulex (Sugawara et al. 1961; Willan 1987; Creese et al. 1997). In Japan, where Musculista is native, the mussel can cause high mortality in the commercially important littleneck clam Venerupis (Ruditapes) philippinarum (Uchida 1965; Crooks pers. obs.), with population explosions of the mussel becoming a local television topic (T. Kikuchi, pers. comm.). Although competition between Musculista and the native cockles appears to be an important factor in the observed declines in these species, potential effects of Musculista must be viewed against other known changes in the system. Addressing these changes also helps explain the recent appearance of C. undatella in the tidal creek, which seems contrary to the results of the experiments. The Northern Wildlife Preserve is now considerably sandier than it was historically, due to dumping of sand on adjacent city beaches (Morrison 1930; Levin 1982; Herring 1991). Chione fluctifraga, which is characteristic of muddier habitats (such as the back of Mission Bay now), has been replaced at this site by C. undatella, which is usually found in sandier habitats (Fitch 1953; Morris et al. 1980; Reish 1995; Crooks, pers. obs). Thus, for C. fluctifraga, both changes in the local sediment regime and the effects of Musculista likely produce a negative response, and it is difficult to assess the relative contribution of each. However, an examination of marsh systems without Musculista (e.g. Tijuana Estuary and Mugu Lagoon; Peterson 1975) and historical conditions in Mission Bay (Morrison 1930; Fitch 1953; MacDonald 1967) suggests that native suspension-feeding surface dwellers such as C. undatella and P. staminea should be more abundant than they currently are. This, coupled with the experimental results, indicates a likely effect of Musculista. The causes of the M. nasuta increase are less clear. Musculista had no significant effect on M. nasuta under experimental conditions (Figure 3), although it is possible that Musculista has had some long-term positive effect on M. nasuta that was not observed in the study. Macoma nasuta might benefit from an
33 increased food supply caused by mussel biodeposition, although food may not be limiting for deposit feeders in this type of environment (Wilson 1991; Kammermans 1993). Also, mussel mats may protect M. nasuta from siphon-nipping fish (e.g. Coen and Heck 1991), such as the long-jawed mudsucker, Gillichthys mirabilis (D. Talley, pers. comm.). Detection of such effects in the current experiment is not possible because of potential cage effects (i.e. increased deposition and protection from fish) in both the treatment and control plots. Macoma nasuta also might have responded to longerterm population cycles or physical changes in the tidal creek not associated with Musculista, although this species is not as typical of sandier sediments as is C. undatella (Reish 1995). Other bivalves have changed in abundance over the last three decades. The subtidal community experienced a decrease in species richness that coincided with a dramatic increase in abundance of Musculista (Figure 2). It is possible that Musculista played a role in this decline, although this is difficult to assess given the limited information on many of the species involved and on subtidal conditions in general. Solen rostriformis, a deep-living suspension-feeder which decreased in abundance in the subtidal (Figure 2), potentially could be negatively affected by Musculista and its mats (Dexter and Crooks 2000). A similar tidal creek species, the jack-knife clam T . californianus, has, however, not declined in abundance since the 1960s. Cryptomya californica, a deep-living species typically found as a commensal in ghost shrimp (Neotrypaea spp.) burrows, appears to have disappeared from the tidal creeks. A bait fishery on ghost shrimp in nearby tidal flats of Mission Bay could have negatively affected C. californica populations (e.g. Peterson 1977). It should be noted that all of these species are deep-dwellers, and it is possible some individuals escaped collection (MacDonald 1967). Implications for restoration and invasion impact assessments A typical goal of restoration is to limit the success of exotics (Zedler 1996), which is clearly difficult in systems with well-established invaders such as Mission Bay. In this study, contemporaneous comparisons of bivalves in the restored and natural creeks showed a trend toward increased representation of the exotic mussels Musculista and Mytilus galloprovincialis (Table 3). These invaders rapidly took advantage
of the newly created creek habitat, achieving relatively high densities and growing to up to two-thirds of their maximum sizes in less than one year. A similar pattern also was reported for Musculista in a restored creek in nearby San Diego Bay (Scatolini and Zedler 1996). In addition to its numerical dominance in restored sites, Musculista may further affect restoration efforts by directly inhibiting native species, such as Chione spp. (Figure 3) or eelgrass (Reusch and Williams 1998). When assessing restoration success, it is considered desirable to compare created sites to reference states which may be distinct in space or time (White and Walker 1997). The bivalve data for the Mission Bay tidal creeks can be used to make several such comparisons. Most recently, bivalves in the restored and natural creeks showed some differences in community structure, although the same species (Musculista) dominated both systems (Table 3). However, data from the 1960s reveal that the bivalve fauna then bears little resemblance to that of the 1990s (Tables 2 and 3). Even the benchmark data from three decades ago is representative of a degraded state, as that intertidal community was distinctly different from the one present 100 years ago (which is assumed to more closely resemble the aboriginal bivalve fauna). If the efficacy of the restoration effort were judged against more recent marsh states without consideration of how the system had changed, this pattern would be a ‘sliding baseline,’ in which degrading systems are used to represent ‘natural’ conditions (Dayton et al. 1998). In this case, it is evident that simple spatial comparisons of reference and restored sites might be misleading because of the dominance of a recognized invader in the natural system. This is a clear indication that baselines have shifted. Given the ever-increasing numbers of exotics in such systems, their potential effects, and difficulties removing them, invasive species must be further considered in the planning and evaluation of restoration efforts (Hedgpeth 1980; Townsend 1991; Palmer et al. 1997). Sliding baselines also become important when assessing the impact of invaders themselves. Failure to consider past biotic assemblages can lead to a biased view of invader effects, as many species already affected might now be absent or rare. For example, recent studies in Mission Bay have demonstrated mostly positive faunal relationships with Musculista (Crooks 1998; Crooks and Khim 1999). However, many of the bivalves with which Musculista may have interacted are now rarely encountered, and it would
34 be difficult to detect the mussel’s deleterious effects without historical records and subsequent manipulative experimentation. The value of historical insight also emphasizes the need to generate comprehensive data on the distribution and abundance of exotic and native species now, for not doing so will compromise the ability to assess future changes in ecosystems. Acknowledgements I thank Alan Johnson-Rivero, Lynn Takata, David Seay, Kevin Crooks, Sarah Maresch, Augusta Anderson, Hugh Khim, Nicole Dederick, Matthias Saladin, Martin Welker, Garen Checkley, Thorsten Reusch and Emma Crooks for their help in the lab and field. Deborah Dexter, Constance Gramlich, Scott Rugh, Carole and Jules Hertz, Ron McConnaughey and Bill Kubitz provided valuable information on bivalves in Mission Bay, and Lisa Levin, Paul Dayton, James Enright, William Newman, David Woodruff, and John Largier provided guidance on the project. The manuscript was improved by comments from Drew Talley, Andrew Chang, James Carlton and three anonymous reviewers. Portions of this research were funded by the E.W. Scripps Foundation, the Mildred Mathias grant of the University of California Natural Reserve System, and a PADI Foundation grant. This paper was also funded in part by a grant from the National Sea Grant College Program, National Oceanic and Atmospheric Administration, U.S. Department of Commerce, under grant number NA66RG0477 project numbers R/CZ-140 and R/CZ-150 through the California Sea Grant College System. This paper is dedicated to the memory of Mia J. Tegner. References Allen BJ (1999) Native eelgrass, Zostera marina, mediates growth and reproduction on an introduced marine bivalve through food limitation. MS Thesis, San Diego State University, California, 64 pp Alpine AE and Cloern JE (1992) Trophic interactions and direct physical effects control phytoplankton biomass and production in an estuary. Limnology and Oceanography 37 (5): 946–955 Andr´e C and Rosenberg R (1991) Adult-larval interactions in the suspension-feeding bivalves Cerastoderma edule and Mya arenaria. Marine Ecology Progress Series 71: 227–234 Byers JE (1999) The distribution of an introduced mollusc and its role in the long-term demise of a native confamilial species. Biological Invasions 1: 339–352
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