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The Prevalence of Non-Indigenous Species in Southern California Embayments and Their Effects on Benthic Macroinvertebrate

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The Prevalence of Non-Indigenous Species in Southern California Embayments and Their Effects on Benthic Macroinvertebrate The prevalence of non-indigenous species in southern California embayments and their effects on benthic macroinvertebrate communities Tim K. Mikel1, Ronald G. Velarde2, J. Ananda Ranasinghe, Stephen B. Weisberg, David E. Montagne3, Donald B. Cadien4, Robert W. Smith5, and Ann Dalkey6 ABSTRACT - The prevalence of non-indigenous species (NIS) in southern California embayments was assessed from 123 Van Veen grab samples collected in nine bays and harbors during the summer of 1998. NIS occurred in all but two samples. They accounted Asian Clam Potamocorbula amurensis invasion of for only 4.3% of the 633 taxa but contributed 27.5% of San Francisco Bay was closely correlated with the the abundance. There was no significant difference in shutdown of the spring plankton bloom (Alpine and the proportion of NIS abundance among ports harbor- Cloern 1992); primary production was transferred ing large vessels, small boat marinas, and areas from the pelagic ecosystem to the benthic ecosystem where boats were not moored. Three species ac- counted for 92% of the NIS abundance: a spionid as a result of suspension feeding by the clam. In- polychaete worm Pseudopolydora paucibranchiata, a tense grazing by the introduced periwinkle Littorina mytilid bivalve Musculista senhousia, and a semelid littorea in Rhode Island affected sediment accumula- bivalve Theora lubrica. The NIS did not appear to have tion and changed the local environment from soft a negative impact at the overall community level since sediments to hard substrate (Bertness 1984). The NIS abundance was positively correlated with the estimated cost of NIS-induced damage has been abundance and richness of other species. This may estimated at $314 billion per year (Pimentel et al. be due to biogenic structures built by P. 2001). paucibranchiata and M. senhousia that enhance the Marine and estuarine systems are particularly abundances of other macrofauna. vulnerable to NIS invasion, stemming, in part, from human-mediated transport of non-native species in the ballast water of ships (Grosholz 2002). Global INTRODUCTION movement of ballast water appears to be the largest Non-indigenous species (NIS) represent a single vector of NIS (Ruiz et al. 1997). Fouling potential threat to the integrity of natural ecosystems. organisms such as barnacles, bryozoans and hydroids, They have been known to change community struc- and wood-boring bivalves are also transported on the ture through elimination of native species, change hulls of ships (Cohen and Carlton 1995). primary production and nutrient cycling, and even Non-indigenous species assessments of marine alter weather patterns (Grosholz et al. 2000). The and estuarine systems on the west coast of the United States have focused mostly on San Francisco 1Aquatic Bioassay and Consulting Laboratories, Inc., 29 North Bay (Carlton 1979, Grosholz 2002). There have been Olive St., Ventura, CA 93001 few assessments of southern California since Carlton 2City of San Diego, 4918 N. Harbor Dr., Ste 101, San Diego, CA (1979) recognized the problem, despite the presence 92106 of some of the world’s largest ports. Los Angeles/ 3County Sanitation Districts of Los Angeles County, P.O. Box 4998, Long Beach Harbor is home to the busiest port in the Whittier, CA 90607 United States, San Diego is a major base for the U.S. Navy, and Marina Del Rey Harbor is the largest 4Private consultant, P.O. Box 1537, Ojai, CA 93024 artificial small craft harbor in the world. Here, we 5City of Los Angeles, Environmental Monitoring Div., 12000 Vista assess the prevalence of NIS in benthic del Mar, Playa del Rey, CA 90293 246 Prevalence of non-indigenous species macroinvertebrate communities of southern California vessel traffic affected the proportion of NIS abun- bays and harbors and their potential impacts on native dance; the arcsine-transformed proportion of NIS communities. abundance was tested among sites in ports, marinas, and other areas. METHODS Benthic samples were collected from 123 sites in RESULTS 9 southern California bays and harbors between July Twenty-seven of the 633 species collected 13 and September 16, 1998. Sampling sites were (4.3%) were NIS. They occurred at 121 of the 123 selected using a stratified random design with port sites and accounted for 27.5% of the abundance. areas that service large ocean-going ships, small boat The percentage of NIS taxa was relatively consistent marinas with recreational vessels, and other areas among the nine bays and harbors (Figure 1, Table 2). where boats were not moored as the strata. At each The abundance of NIS was more variable and also sampling site, sediment samples for benthic infaunal showed no pattern with respect to size or the type of analysis were collected using a 0.1 m2 Van Veen grab vessel traffic. There was no significant difference in and sieved through a 1 mm mesh screen. Only the relative abundance of NIS between ports, mari- samples penetrating at least 5 cm into the sediment nas, and other areas. and with no evidence of washout or slumping were Three species (Pseudopolydora processed. Material retained on the screen was paucibranchiata, a spionid polychaete worm; placed in a relaxant solution of 1 kg MgSO4 or 30 ml Musculista senhousia, a mytilid bivalve; and Theora propylene phenoxytol per 20 L of seawaterfor at least lubrica, a semelid bivalve) accounted for 91% of 30 minutes and preserved in 10% sodium borate NIS abundance (Table 3). P. paucibranchiata was buffered formalin. In the laboratory, specimens were the most abundant species at five embayments transferred to 70% ethanol, sorted, identified to the (Channel Islands Harbor, Dana Point Harbor, Los lowest practical level (most often species), and Angeles/Long Beach Harbor, Marina Del Rey, and enumerated. Mission Bay) and M. senhousia at two embayments We adopted the techniques and definitions of (Newport Bay and San Diego Harbor); T. lubrica Lindroth (1957), Carlton (1979), Chapman (1988), was the abundance dominant only in Anaheim Bay. Chapman and Carlton (1991, 1994), and T N & The NIS abundance was strongly and positively Associates Inc. (2001) to identify NIS on our species correlated with total abundance and numbers of list based on their taxonomy, biology, and history of species (Table 4). The strongest relationship was occurrence in southern California (Table 1). Native with total abundance (r = 0.72). The correlation with (indigenous) species are populations occurring within number of taxa was weak (r = 0.39) although signifi- their natural range and without the aid of human cant. activities (T N & Associates Inc. 2001). The NIS To assess effects on native and cryptogenic are populations outside their natural range that were species, the correlation between NIS abundance and introduced intentionally or accidentally by humans. community abundance was repeated with NIS Introduced species are defined as reproductive subtracted from the total abundance. The correlation populations of species or subspecies established by was still positive (r = 0.52) and significant. There human activities outside their previous natural range. was also a significant positive correlation between Cryptogenic organisms are neither demonstrably NIS abundance and the number of native and crypto- native nor introduced (Cohen and Carlton 1995). genic species (r = 0.34). To assess whether the NIS had an effect on benthic communities, we used correlation analysis to quantify associations between NIS abundance and DISCUSSION two community measures: total abundance and Embayments in southern California are highly number of taxa. The analysis was repeated with NIS invaded by non-native macrofauna with NIS encoun- removed to assess the effects on native and crypto- tered at 121 of 123 sites. More than a quarter of the genic species only. All measures were log-trans- animals collected were non-indigenous. Relative formed prior to correlation analysis. The analysis of abundances in San Francisco Bay, the only west variance (ANOVA) was used to assess whether coast area that has been intensively studied, are even Prevalence of non-indigenous species 247 Table 1. Non-indigenous species in southern California embayments. Nomenclature follows SCAMIT (2001). *= First report of taxon as NIS. Taxon Original Locality References Annelida: Polychaeta Brania mediodentata* Galapagos Westheide 1974 Diplocirrus sp. SD1* Probably Arctic Rowe 1998; Ruff 1996 Eteone aestuarina* El Salvador Hartmann-Schroder 1959 Neanthes acuminata Unknown T N & Associates Inc. 2001 Nephtys simoni* Florida Hilbig 1994 Polydora cornuta U.S. east coast T N & Associates Inc. 2001 Pseudopolydora paucibranchiata Japan T N & Associates Inc. 2001; Carlton 1979 Streblospio benedicti U.S. east coast Carlton 1979 Syllis (Typosyllis) nipponica Japan T N & Associates Inc. 2001 Arthropoda: Crustacea: Amphipoda Aorides secundus Japan Cohen et al. 2002 Caprella natalensis Unknown T N & Associates Inc. 2001 Eochilidium sp. A Unknown T N & Associates Inc. 2001 Grandidierella japonica Japan T N & Associates Inc. 2001; Chapman and Dorman 1975 Liljeborgia sp. (red/white fouling) Unknown Cohen et al. 2002 Listriella sp. A* Unknown SCAMIT 1987 Paradexamine sp. SD1* Unknown Pasko 1999 Sinocorophium heteroceratum Western Pacific (China) Chapman and Cole 1994; T N & Associates Inc. 2001 Arthropoda: Crustacea: Isopoda Paracerceis sculpta Unknown T N & Associates Inc. 2001 Arthropoda: Crustacea: Mysidacea Deltamysis sp. A* Unknown Possibly D. holmquistae Bowman and Orsi 1992 Mollusca: Bivalvia Musculista senhousia Japan T N &
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