Biological Invasions (2005) 7: 369–392 Springer 2005
Trends in marine biological invasions at local and regional scales: the Northeast Pacific Ocean as a model system
Marjorie J. Wonham1,2,* & James T. Carlton3 1Department of Zoology, University of Washington, Box 351800, Seattle, WA 98195-1800, USA; 2Current address: Centre for Mathematical Biology, Department of Biological Sciences and Department of Mathematical & Statistical Sciences, University of Alberta, CAB 632, Edmonton, AB, Canada T6G 2G1; 3Maritime Studies Program, Williams College-Mystic Seaport, P.O. Box 6000, Mystic, CT 06355, USA; *Author for correspondence (e-mail: [email protected]; fax: +1-780-492-6826)
Received 17 September 2003; accepted in revised form 8 March 2004
Key words: ballast water, Crassostrea, introduced species, invasion rate, invasion success, non-native species, Pacific Northwest
Abstract
Introduced species are an increasing agent of global change. Biogeographic comparisons of introduced biotas at regional and global scales can clarify trends in source regions, invasion pathways, sink regions, and survey effort. We identify the Northeast Pacific Ocean (NEP; northern California to British Colum- bia) as a model system for analyzing patterns of marine invasion success in cool temperate waters. We review literature and field surveys, documenting 123 introduced invertebrate, algal, fish, and vascular plant species in the NEP. Major invasion pathways were shipping (hull fouling, solid and water ballast; 1500s-present) and shellfish (particularly oysters) and finfish imports (commonest from the 1870s to mid- 1900s). The cumulative number of successful invasions over time increased at linear, quadratic, and exponential rates for different taxa, pathways, and regions within the NEP. Regional analysis of four major NEP estuaries showed that Puget Sound and the contiguous Straits had the most introduced spe- cies, followed by Humboldt Bay, Coos Bay and Willapa Bay. Data on cumulative shipping volumes pre- dicted smaller-scale, but not larger-scale spatial patterns in the number of shipping-mediated invasions. We identify the major challenges in scaling up from regional to global invasion analysis in cool temper- ate regions. Retrospective analyses for distinct biogeographic regions such as the NEP provide insight into vector dynamics and regional invasibility, and are a necessary foundation for monitoring and man- aging global change caused by biotic invasions.
Introduction regional and global scales: this variation is the complex product of differences in the history, tim- Biological invasions are a major agent of global ing, and diversity of transport vectors, traits of the change (Ruiz et al. 1997; Vitousek et al. 1997; Sala introduced species, abiotic and biotic features of et al. 2000). In cool-temperate coastal communi- the invaded environment, and sampling strategies. ties, invasions by non-native marine and estuarine Biogeographic comparisons, based on a historical species are increasing around the world (Pollard and geographic synthesis of the introduced biota and Hutchings 1990a, b; Eno et al. 1997; Cohen within and between regions, can help elucidate the and Carlton 1998; Leppa¨koski and Olenin 2000; relative importance of these factors. Ruiz et al. 2000a; Levings et al. 2002). The number As a model system to analyze the growing and diversity of non-native species vary at both number of invasions in cool temperate marine 370
200 km Hecate Strait BRITISH Queen COLUMBIA Haida Charlotte Gwaii Sound (Queen Strait of Charlotte Georgia Islands) V an co uv er Vancouver Canada USA Strait of Juan de Fuca
Puget Sound Seattle Pacific WASHINGTON Willapa Bay Ocean
OREGON Coos Bay
Humboldt Bay
Cape Mendocino CALIFORNIA
Figure 1. Major coastal water bodies of the cool temperate Northeast Pacific Ocean (Cape Mendocino, California, USA, to Haida Gwaii (Queen Charlotte Islands), British Columbia, Canada) treated in this review. ecosystems, we selected a 3000 km coastal ern limit of the Northern California Current Eco- biogeographic region in the Northeast Pacific region (OOPAC 1994), while the Queen Ocean (NEP) extending from Cape Mendocino, Charlottes represent the northern limit of contig- California (40 26.4¢ N, 124 24.3¢ W) to Haida uous coastal surveys before the considerably Gwaii (Queen Charlotte Islands), British Colum- more northern Alaskan datasets. We synthesized bia, (52–54 N, 131–133 W) (Figure 1 and records of introduced marine and estuarine spe- Table 1). Cape Mendocino represents the south- cies in this region and analyzed patterns in their
Table 1. Regions within the Northeast Pacific treated in this analysis. Region Definition Abbreviation Puget Sound and Contiguous coastal waters of the Juan de Fuca Strait (entrance 48 23¢ N, SS Straits, WA and BC 124 44¢ W) and Puget Sound north to Hecate Strait (entrance 54 23¢ N, 132 26¢ W); includes Skeena, Fraser, Skagit, and Snohomish River estuaries and Duwamish waterway Coos Bay, OR Coos Bay (entrance 43 22¢ N, 124 22¢ W) including Coos River estuary CB Willapa Bay, WA Willapa Bay (entrance 46 37¢ N, 124 01¢ W) including Willapa, Palix and WB Naselle River estuaries Humboldt Bay, CA Humboldt Bay (entrance 40 23¢ N, 124 44¢ W) including Trinity, Eel, HB and Mad River estuaries Other Additional locales between Cape Mendocino and Haida Gwaii, including Other Yaquina Bay, OR, Columbia River Estuary, WA/OR, and Grays Harbor, WA) The total coastline treated here extends from Haida Gwaii, British Columbia (BC), Canada ( 54 N), through Washington (WA) and Oregon (OR) to Cape Mendocino, California (CA), USA ( 40 N). 371 taxonomic distribution, origins, invasion path- the late-1800s, iron-hulled ships coated with anti- ways, temporal trends, and regional distributions. fouling paint provided much less substrate for Lessons from regional-scale analysis of portions hull-fouling organisms. In lieu of solid ballast of the NEP highlight the challenges of making these ships carried water, and since its required global-scale comparisons. separation from oily bilge in the 1980s ballast water has served as a less polluted pathway for liv- Northeast Pacific invasion pathways ing organisms (Carlton 1985; Carlton and Geller 1993; Carlton and Hodder 1995). Although ship- Humans have inhabited the NEP coastline for ping tonnage is not necessarily a direct indicator thousands of years, but it was the 16th-century of number of ships or volume of ballast water, we arrival of European explorers and colonizers that use it as an indicator of the relative scale of ship- ushered in the present era of human-mediated ping pathways through time in the NEP. marine biological invasions. Dominant marine Shellfish imports to the NEP began in the late invasion pathways in the NEP have included ship- 1800s. The Atlantic oyster Crassostrea virginica ping (hull fouling, solid ballast, and water ballast) was imported from the 1880s to the 1930s. Paci- and imports for aquaculture and fisheries fic oysters, primarily C. gigas, were imported (reviewed by Carlton 1985, 1987; Hitchman 1990). from Japan beginning in the early 1900s and Shipping introductions presumably began with peaking around the 1950s; today experimental the arrival of European ships via the South imports are conducted only occasionally (D. Che- Atlantic and South Pacific in the mid-1500s, and ney, Director, Pacific Shellfish Institute, Olympia, Russian ships from the west and north Pacific in WA, USA, pers. comm.). Both oyster species the 1700s. Traffic increased during the gold rush served as invasion pathways for additional hitch- of the mid-1800s and again following the 1914 hiking invertebrates and algae (Quayle 1964, opening of the Panama Canal. In the US, 1988; Carlton 1979). Successful intentional intro- increased traffic was evident in the major ports of ductions have included several additional bivalve Puget Sound (Seattle and Tacoma); in ports of species; other molluscs and crustaceans were the outer coast, shipping remained at lower levels released but failed to establish (Carlton 1979). and in some areas has decreased in recent dec- Finfish were introduced intentionally to brackish ades (Figure 2). Early ships carried organisms on and coastal waters of the NEP in the late 1800s and in their wooden hulls and in solid ballast. By and early 1900s (Smith 1896; Fuller et al. 1999).
108
107
106
105 Shipping traffic (Short Tons)
104 1890 1910 1930 1950 1970 1990 2010 Year
Figure 2. Annual shipping tonnage reported for selected years in selected Northeast Pacific ports: Humboldt Bay, California (solid squares), Coos Bay, Oregon (open triangles), Willapa Bay, Washington (open circles), and the Puget Sound ports of Seattle and Tacoma, Washington (solid diamonds). Note log scale. 372
Other potential invasion pathways that are less Atlantic salmon Salmo salar and the Mediterra- well documented include intentional and inadver- nean mussel Mytilus galloprovincialis). Although tent releases associated with the aquarium trade, the excluded species may in some cases play bait shipment, and planting and transplantation important ecological roles in marine and estuarine of eelgrass and salt marsh grasses. communities, our focus was on the changing com- position of established species living and repro- Materials and methods ducing in the these environments.
In this review we synthesized current and histori- Data classification cal literature including peer-reviewed scientific publications, government reports, and unpub- Species were classified as native or introduced lished data. Field records from surveys by the based on criteria in Chapman (1988) and Chap- authors (JTC 1978–1979; MJW 1995–2000) and man and Carlton (1991). We included only those Cohen et al. (1998, 2001) were also included. non-native species believed to have established (From the 2001 survey by Cohen et al., we self-maintaining populations in the NEP. Records include only records of invader range extensions of cryptogenic species (sensu Carlton 1996) and within the NEP.) We treated marine and estua- species that have been reported but are not rine invertebrates, algae, fishes, and vascular believed to be established were excluded. Species plants as completely as possible. We noted but were further classified according to their region of did not cover in detail certain invasions by phy- origin (Table 2), invasion pathway (Table 3) and toplankton and coastal insects since records for date of invasion. Region of origin was assigned these groups were sparse. Habitat coverage based on literature reports of native ranges; for extended to marine and brackish waters, and for some now-cosmopolitan species, the region of ori- angiosperms included salt-water flooded habitats. gin is not yet known. We excluded the following groups of intro- We assigned species to their most probable inva- duced species: strictly terrestrial plants that invade sion pathways based on our knowledge of trans- along the edges of salt marshes, dunes, beach cliffs port vectors, the location of an invader’s initial and bluffs (e.g., beachgrass Ammophila arenaria discovery (e.g., oyster beds during the height of and iceplant Carpobrotus edulis), terrestrial ani- oyster introductions and prior to ballast water mals that venture into the intertidal to feed (e.g., coming into common use), and general knowledge Norway rats Rattus norvegicus), fish that may be of its habitat and life history. For many species, found, but do not reproduce in brackish waters several pathways were plausible: these were con- (e.g., carp Cyprinus carpio and mosquitofish Gam- servatively assigned to a ‘multiple pathway’ cate- busia holbrooki), freshwater species that may occa- gory. Invasion date was taken as the date of sionally occur as adults in waters contiguous with planting or release, where known; otherwise, date tidal brackish waters (e.g., Asian clam Corbicula of first collection was used. This last should be manilensis), and records of marine species that interpreted with care since a species may have been reproduce in our region but are not known to be discovered considerably after the (unknown) date established independently of aquaculture (e.g., of its first arrival. When the original author did
Table 2. Biogeographic origins of established non-native marine and estuarine species in the Northeast Pacific. Origin Definition Abbreviation Species No. % Western Pacific N. Pacific coast of Asia: Japan, Korea, China WP 43 35.0 Western Atlantic Atlantic coast of N. America (including Gulf of Mexico) WA 32 26.0 Eastern Atlantic Atlantic coast of Europe north of Spain EA 10 8.1 North Atlantic N. Atlantic Ocean (i.e. northern EA and WA combined) NA 15 12.2 Ponto-Caspian Azov, Caspian, and Black Seas PC 2 1.6 Southern hemisphere S. Pacific, S. Atlantic, and Indian Oceans SH 9 7.3 Unknown Origin cannot be assigned with confidence UNK 12 9.8 373
Table 3. Invasion pathways of established non-native marine and estuarine species in the Northeast Pacific. Pathway Transport Abbrevia- Species tion No. % Ballast water Carried in ballast (not bilge) water taken aboard by vessels BW 16 13.0 for trim and stability; includes sediments in tanks Dry ballast Carried with ships’ solid ballast of rocks and sand (mostly DB 1 0.8 maritime plants and animals) Ship fouling Attached to or boring into wooden ships SF 10 8.1 Commercial Associated with introductions of Atlantic (AO) or Pacific CO 25 20.3 oyster industry (PO) oysters (AO/PO) Intentional plantings Deliberately released for a variety of purposes, including IP 8 6.5 marsh restoration, erosion control, cattle forage, and gardens (excludes CO) Commerce Accidentally released from transport of fisheries, soil, CM 2 1.6 plants, etc. (excludes CO) Multiple Two or more of BW, SF, or CO are likely pathways BW/SF/CO 53 43.1 Unknown Likely pathway could not be assigned with confidence UNK 8 6.5 not report a collection date (approximately 15% of particular (Carlton 1979, unpublished data; Cohen species), we used the publication date of the first et al. 1998, 2001; Boyd et al. 2002). The following record; to reduce the associated bias, these records description of each area is summarized from sev- were omitted from temporal data analyses. When eral sources (Carlton 1979; Hitchman 1990; Ency- the first collection record was reported only as a clopedia Britannica 2001; PNCERS 2001; Army decade (e.g., 1960s), we used the middle year of Corps of Engineers Navigation Data Center, the decade (e.g., 1965) for analysis. Waterborne Commerce Statistics Center
C. gigas culture makes Willapa one of the largest transformed data), and an exponential model rep- commercial oyster-export regions in the United resenting an accelerating rate of successful inva- States. sions (linear fit to ln(x)-transformed data). R2 Coos Bay is the largest estuary in Oregon, cov- values were compared to select the best fit among ering approximately 4920 ha at high tide. The city the three models. Temporal trends for the multiple of Coos Bay, first settled by Europeans in 1854, and oyster-mediated invasion pathways, and in the became a major coal and lumber port; lumber Coos Bay region, approximated a sigmoidal curve. remains the major export, although shipping has However, in the absence of a mechanism to justify declined in the last two decades. Historical C. virg- this increased-parameter fit, we used the three sim- inica plantings are reported anecdotally in Coos pler models to allow ready comparison across Bay. C. gigas was first planted in the 1930s and datasets. continues to be imported from other NEP bays. Temporal regressions were conducted for all Humboldt Bay, the second largest estuary in species together and for the following 11 sub- California, covers approximately 20,000 ha at analyses: molluscs only, Pacific and Atlantic ori- high tide. The bay was first explored and settled gins, ballast water, oyster, shipping, and multiple by Europeans in 1850; it became an important pathways, and the four NEP regions. In each lumber and passenger port but shipping has analysis, all three models explained the variance remained at a low volume since the turn of the relatively well, with R2 > 0.73, and both the century. C. virginica was planted in the bay from complete and reduced datasets were best fit by 1896 to 1930s. C. gigas was planted from 1953 the same model type. Only the best-fit model for onwards, and continues to be cultured here. the reduced dataset is reported. For comparisons across the 4 NEP regions, 6 Data analysis invertebrate and 1 diatom species reported only from other NEP locations were excluded from Introduced species counts were analyzed for distri- the original 108, leaving 101 species. We used v2 butional patterns and temporal trends by taxo- tests compared species number, origin, invasion nomic group, region of origin, and invasion pathway, and cumulative shipping volume in pathway, and across NEP regions. Maritime short tons from 1900 to 2000 across regions. For plants, whose arrival dates were largely unknown, Willapa Bay, the shipping analysis extended only and fish, which are unique in our dataset in being to 1970, the last year of shipping records. All almost exclusively intentionally introduced, were analyses were conducted with the statistical pack- excluded from temporal and regional analyses age JMP Version 3.1 for Macintosh ( SAS leaving 108 marine invertebrate, algal and plant Institute 1988–1999) and used a significance level species. of a ¼ 0.05. For temporal analyses, species counts were regressed against year since 1900, since data reso- lution before then was poor. The two earliest mol- Results luscan invasions were thus omitted, leaving 106 species. Analyses were conducted with the com- We documented a total of 123 introduced marine plete dataset and with a reduced dataset of collec- and estuarine species established in the NEP tion dates only (i.e., omitting records where only (Appendices 1 and 2). These consisted of 99 mar- the publication date was known) to reduce the ine invertebrates, 4 marine algae, 14 marine and effects of reporting bias. For both datasets, we maritime plants, and 6 marine and brackish-water compared three alternative models to describe the fish. All taxa were identified to species except for change in the cumulative number of successful five invertebrates identified only to genus. reported invasions over time: a linear model repre- senting a constant rate of successful invasions (fit Taxonomic distribution to untransformed data), a quadratic polynomial model representing a constant increase in the rate Introduced invertebrates were distributed over 10 of successful invasions (linear fit to square-root phyla (Appendix 1). Together, arthropods, mol- 375 luscs and annelids made up over half the species. 100 A Arthropods (n ¼ 32 species) consisted primarily All taxa of amphipods (12) and copepods (7). Molluscs 75 (n ¼ 27 species) consisted equally of bivalves (14) 50 and gastropods (13). Annelids (n ¼ 13 species) consisted of polychaetes (8) and oligochaetes (5). 25 Molluscs In addition, bryozoan (8), cnidarian (7), ascidian Cumulative no. species (5), sponge (3), flatworm (2), foraminiferan (1), 0 and kamptozoan (1) species were reported 0 20406080100 (Appendix 1). 60 Algal records consisted of one brown macro- B Multiple alga, two red macroalgae, and one diatom pathways (Appendix 1). Plants consisted of two marine 40 genera, the cordgrasses Spartina spp. (four spe- cies) and the eelgrass Zostera japonica, and nine 20 Ballast water maritime species from saltmarsh and strand habi- tats (Appendix 2). Fishes included two coastal Cumulative no. species 0 marine species (American shad Alosa sapidissima 0 20406080100 and striped bass Morone saxatilis) and four estu- arine species (Appendix 2). 30 C Commercial The earliest records of introduced species in oysters the NEP are the fishes A. sapidissima and 20 M. saxatilis and the molluscs Myosotella myoso- tis and Mya arenaria, all first reported in the 10 1870s–1880s (Carlton 1979) (Appendices 1 and Ship
2). Beginning in the early 1900s, species records Cumulative no. species fouling began to accelerate (Figure 3a and Table 4). This 0 increase is the product of trends in the number 0 20406080100 Year since 1900 of introductions, invasion success, and species collection. To attempt to distinguish among these Figure 3. Cumulative number of established non-native mar- contributing factors, we repeated the temporal ine and estuarine species in the Northeast Pacific, by date of analysis for molluscs, a conspicuous and well- first record, for different taxa and invasion pathways. (A) All invertebrates and algae together (solid diamonds), and mol- studied group that might be expected to suffer luscs only (open diamonds); (B) multiple invasion pathways less reporting bias than other taxa (Carlton 1999; (likely via one or more of ballast water, ship fouling and com- Ruiz et al. 2000a). Cumulative mollusc records mercial oysters; solid diamonds) and ballast water only (open increased linearly over time, showing no apparent diamonds); (C) commercial oyster (solid diamonds) and ship acceleration (Table 4 and Figure 3a). We also fouling (open diamonds) invasion pathways (see Table 4 for regression equations). investigated the contribution of recent intensive field surveys to the accelerating pattern. How- ever, these surveys (Carlton 1979; Cohen et al. southern hemisphere (7%), and only two from 1998) each added only two new invader records the Ponto-Caspian region (Table 2 and Appendix to the overall region and did not change the 1). Over time, both Atlantic and Pacific records qualitative shape of the curve. increased at similar rates (Table 4). By far the majority of species were introduced Origins and pathways unintentionally (87%); only a small percentage were intentionally imported (6%) (Table 3). For The majority of invaders were native to the 50% of species, it was possible to assign a single northern hemisphere (Table 2). Approximately most probable invasion pathway. The three com- half originated in the Atlantic (46%) and one- monest pathways, all unintentional, were Pacific third in the Pacific (35%). Fewer came from the and Atlantic oyster shipments (20% of all 376
Table 4. Regression equations for number of established non-native marine and estuarine species reported in the Northeast Pacific vs year since 1900, by taxon, region of origin, invasion pathway, and geographic subregion. Analysis Model a SE b SE R2 Taxa All Quadratic 0.65 0.05 0.087 0.001 0.995 Molluscs Linear )0.45 0.30 0.199 0.005 0.989 Origin Atlantic Quadratic 0.48 0.11 0.054 0.001 0.979 Pacific Quadratic 0.41 0.10 0.057 0.001 0.982 Pathway Ballast water Exponential )9.70 1.02 0.124 0.011 0.947 Multiple Exponential )0.07 0.10 0.041 0.001 0.967 Oysters Linear )0.82 0.75 0.264 0.014 0.949 Ships Linear )0.81 0.63 0.106 0.009 0.953 Subregion Straits and Sound Quadratic 1.06 0.08 0.064 0.001 0.986 Willapa Bay Quadratic 0.03 0.24 0.056 0.003 0.934 Coos Bay Quadratic )3.65 0.28 0.109 0.003 0.975 Humboldt Bay Exponential )0.53 0.14 0.041 0.002 0.967 Model is best-fit linear regression to untransformed (Linear: y=a+bx), square-root(x)-transformed (Quadratic: y=(a+bx)2), or ln(x)-transformed (Exponential: y=exp(a+bx)) data. SE, 1 standard error for estimate of a and b. All models significant at P < 0.000l. species), ballast water transport (13%), and ship tive number of invasion records accelerated in fouling (8%). For nearly all the remaining spe- all regions, with a quadratic increase in three of cies, multiple inadvertent pathways appeared the four regions and an exponential increase in equally likely (43%) (Table 3). Other documented Humboldt Bay (Figure 4 and Table 4). In the invasion pathways were dry ballast, and the com- Straits and Sound, Willapa Bay, and Humboldt mercial movement of species other than oysters Bay, the same model type remained the best fit (Table 3 and Appendix 1). Cumulative species even when new records from recent surveys for records attributed to ballast water and to multi- introduced species (Cohen et al. 1998, 2001; ple pathways accelerated over time, whereas Boyd et al. 2002) – which might create an those attributed to oysters and other shipping apparent recent increase in successful invasions vectors (hull fouling and solid ballast) increased – were omitted from analysis. This analysis was linearly (Figures 3b, 3c and Table 4). not repeated in Coos Bay, as there are no recently published surveys of invaders from that Regional differences region. Dominant invasion pathways differed signifi- Among regions, the most invaders were reported cantly among regions (v2 ¼ 20.0, df ¼ 9, P ¼ from the Straits and Sound (76 species) and 0.02) (Table 6). Two of the regions had 2.5–5 fewer from Humboldt (54), Coos (52), and Wil- times as many oyster-mediated as shipping-medi- lapa (43) Bays (Table 5). Approximately half ated invaders, whereas Coos Bay – which had the the species in these three bays were also found highest proportion of ballast-mediated and the in the Straits and Sound (50–53%), whereas the lowest proportion of oyster-mediated invasions – bays had a broader range in overlap of 43–65% showed the opposite pattern. Willapa Bay and among them (Table 5). Over time, the cumula- the Straits and Sound had the highest proportion
Table 5. Established non-native marine and estuarine species in four Northeast Pacific subregions. Straits and Sound Willapa Bay Coos Bay Humboldt Bay Straits and Sound 76 88.4 (38) 76.9 (40) 70.4 (38) Willapa Bay 50.0 (38) 43 50.0 (26) 51.9 (28) Coos Bay 52.6 (40) 60.5 52 63.0 (34) Humboldt Bay 50.0 (38) 65.1 (28) 65.4 (34) 54 Number of species (out of total 108) shown for each region on diagonal. Percent (and number) of species in row site shared by col- umn site shown above and below diagonal. 377
75 A Commercial cargo tonnage in the Straits and Straits & Sound region has increased dramatically over Sound 50 time, whereas in Coos Bay and Humboldt Bay it has remained steadier and shipping in Willapa Bay has ceased altogether (Figure 2 and Table 6). We 25 qualitatively compared cumulative shipping ton- Willapa nage to the total number of invaders across
Cumulative no. species Bay 0 regions for two sets of pathways, probable ship- 0 20406080100 ping (i.e., BW+SF) and possible shipping (i.e., BW+SF plus multiple-pathway invaders assigned 75 B to BW, SF, or both) (Table 6). In both analyses, Coos the Straits and Sound had fewer invaders via these 50 Bay pathways (n ¼ 52) than would be predicted by its shipping traffic, whereas the other ports had more. 25 Willapa Bay had the fewest such species (n ¼ 31) Humboldt and the least shipping tonnage. Coos Bay and
Cumulative no. species Bay 0 Humboldt Bay had similar species counts via these 0 20406080100 pathways (49 and 44, respectively), but Coos Bay Year since 1900 had an order of magnitude more tonnage. The Figure 4. Cumulative number of established non-native mar- proportion of invaders from Atlantic vs Pacific ine and estuarine species in the Northeast Pacific, by date of oceans did not differ significantly among NEP 2 first record in four Northeast Pacific regions: (A) Puget Sound regions (v ¼ 1.7, df ¼ 3, P ¼ 0.63) (Table 6). and Straits (solid diamonds) and Willapa Bay (open dia- Nineteen species were reported in all four monds); (B) Coos Bay (solid diamonds) and Humboldt Bay regions, and thirty-eight species were reported (open diamonds) (see Table 4 for regression equations). from only one region in our analysis (although some of these have also been recorded as invad- ers outside the NEP; Carlton 1979, 1987, 1992). of oyster-mediated invasions; Willapa had the These unique records were most common in the lowest proportion of ballast-water and ship-foul- Straits and Sound (28% of species), moderately ing invasions. The proportion of multiple-path- so in Humboldt (15%) and Coos Bays (12%), way invasions was greatest in Coos Bay and and least common in Willapa Bay (7%) lowest in the Straits and Sound (Table 6). (v2 ¼ 11.3, df ¼ 3, P ¼ 0.010) (Table 6).
Table 6. Invasion pathways and origins of established non-native marine and estuarine species in four Northeast Pacific regions. Straits and Sound Willapa Bay Coos Bay Humboldt Bay Pathway (%) Commercial oysters 31.2 31.1 5.8 16.4 Ship fouling 6.5 4.4 9.6 10.9 Ballast water 6.5 2.2 9.6 5.5 Multiple 54.3 62.2 75.0 63.6 Origin (%) Atlantic 42.9 44.4 44.2 47.3 Pacific 45.5 44.4 30.8 32.7 Southern hemisphere 0 0 5.8 7.3 Unknown 9.1 8.9 17.3 10.9 Total no. species 77 45 52 55 No. unique species 22 3 8 8 Shipping tonnage 1823 35 259 65 Total and unique number of established invaders, and cumulative shipping tonnage in millions of short tons from 1900 to 1999 (see Figure 2), also given. 378
Species reported in all four regions included the among different groups of organisms, to vary Pacific oyster Crassostrea gigas, and fourteen spe- with the original authors’ methods and intent, cies of anemone, polychaete, mollusc, crustacean, and to increase as the introduced population bryozoan and tunicate all associated with multiple grows. Since our data were gleaned from a wide invasion pathways including commercial oyster range of sources spanning more than a century shipments. Like C. gigas, the Atlantic oyster of reporting, certain detection biases may be C. virginica was introduced to all four regions; expected among taxa, among regions, and over unlike its congener, C. virginica remains estab- time, contributing to the overall patterns lished only in the Straits and Sound. Several other observed. We discuss the observed patterns in species introduced via oyster shipments are invasion records in the context of these biases. reported only from this region, including the pred- atory flatworm Pseudostylochus ostreophagus, biv- Taxonomic distribution alves Musculista senhousia and Lyrodus takanosimensis, and gastropods Crepidula convexa, Most of the invaders we report are invertebrates; Nassarius fraterculus, and Batillaria attramentaria. fewer are plants or fish, fewer still are algae, and One macroalga, Gelidium vagum, was reported we found no unambiguous records of introduced only from the Straits and Sound. Cordgrasses protists. This pattern is generally consistent with Spartina anglica and S. patens are also found that of other coastal regions (Cohen and Carlton only in this region, while S. densiflora is reported 1995; Ruiz et al. 2000a). Plants and fish, how- only from Humboldt Bay. Other relatively con- ever, are conspicuous taxa in which we might spicuous species established in single regions expect invasions to be readily detected. The low include the clam Gemma gemma and the crab number of plant records in this review is perhaps Carcinus maenas in Humboldt Bay, the clam Pet- not surprising since comparatively few vascular ricolaria pholadiformis in Willapa Bay, and the species thrive in saltwater habitats. For fish, crab Rithropanopeus harrisii and opisthobranchs which are clearly capable of successful transport Philine auriformis and Tenellia adspersa in Coos and invasion in marine waters (Golani 1996; Bay. The wood-boring isopod Limnoria tripuncta- Wonham et al. 2000), their low numbers in ta is found in the Straits and Sound, Willapa coastal North America may reflect a historical Bay and Coos Bay, whereas its congener L. quad- tendency to intentionally introduce freshwater ripunctata is reported only in Humboldt Bay. rather than marine species (Moyle 1986; Fuller et al. 1999). The conspicuously low number of macroalgae Discussion may indicate genuinely low invasion opportunity or success, or may reflect sampling biases in both We report 123 introduced established marine and pathway and field surveys (Carlton and Geller maritime species in the Northeast Pacific. This is 1993; Cohen et al. 1998; Smith et al. 1999). The an underestimate, since some invaders have likely ever-finer taxonomic resolution of macroalgae in become established but have not yet been discov- this region (e.g., Hayden 2001) may ultimately ered, or have been collected but not yet recog- identify certain cosmopolitan species as non- nized as introduced. The observed temporal and native. For groups such as protists and phyto- spatial patterns in invasion records are necessar- plankton, which have been reported at high den- ily the product of patterns in introductions, inva- sities in ballast water (Subba Rao et al. 1994; sion success, and detection (Cohen and Carlton Galil and Hulsmann€ 1997; Ruiz et al. 2000b), the 1998; Ruiz et al. 2000a; Costello and Solow paucity of records almost certainly reflects a 2003). The chances of an invader being initially strong sampling bias resulting from their small introduced are likely to have peaked in the past size and generally less well-known taxonomy and for certain pathways (e.g., oyster imports, hull distribution. fouling) but to be increasing for others (e.g., The major invertebrate phyla absent from our unregulated ballast water release). The chances dataset are echinoderms, ctenophores, nema- of an invader being detected are likely to differ todes, and nemerteans. Since echinoderms and 379 ctenophores are generally conspicuous species, report an accelerating increase in cumulative their absence may indeed reflect low invasion invader records that is consistent with patterns success, stemming from low opportunity (i.e., observed in other regions (Cohen and Carlton low propagule pressure) or low success upon 1998; Ruiz et al. 2000a; Leppa¨koski and Olenin release. For the more cryptic nematodes and 2000). Linear and polynomial models fit most of nemerteans, sampling and taxonomic biases likely our datasets the best, implying constant and line- play a large role in their apparent absence. arly increasing rates of successful reported inva- sions, respectively. Two sets of records, the Origins and pathways multiple-pathway and ballast-mediated invasions, were fit slightly better with an exponential model, The majority of documented invaders in the NEP indicating an accelerating rate of successful docu- are native to the northern hemisphere, which mented invasions. reflects the historical dominance of Asian, Euro- The rate of increase in invasion records must pean, and eastern North American trade to this be interpreted with caution. Sampling methods, region. While the overall number of reported habitats, and geographic and taxonomic special- invaders is an underestimate, the number of invad- ties of the original authors can all affect invasion ers from the western Pacific is even more so, since record rates (e.g., Ruiz et al. 2000a). This diffi- most invertebrate and algal species with trans- culty applies to the oyster-mediated invasions dis- Pacific distributions have not yet been analyzed cussed above and is even more acute for with molecular tools to determine their origins. shipping-mediated invasions, which could have Although the ship fouling and commercial oys- begun as early as the mid-1500s. Since regional ter pathways are far more restricted today than surveys of the biota did not begin until the mid- they were historically, some recent records were or even late-1800s, the intervening 300-year assigned to these pathways, such as the trematode period remains virtually unresolved. Cercaria batillariae (2000s), the polychaetes Nean- Records of molluscs, which may suffer some of thes succinea (1980s) and Sabaco elongatus (1990s), the least collection bias of all taxonomic groups the clam Gemma gemma (1990s), and the bryozoan (Carlton 1999, Ruiz et al. 2000a), may provide a Bugula stolonifera (1990s) (Appendix 1). The first ‘truer’ picture of invasion patterns. Unlike the four we regard as oyster-associated invasions that overall trend, NEP mollusc invasions increased were either overlooked earlier or spread recently steadily and did not appear to accelerate. This by intracoastal vectors or natural dispersal. pattern is consistent with mollusc records in B. stolonifera may have been overlooked in the other regions (Ruiz et al. 2000a). More data are past, or may be a recent ship-mediated invasion. required for other individual taxonomic groups Approximately half the invaders were readily (such as polychaetes, bryozoans, or algae) to assigned to a single invasion pathway. For nearly determine whether molluscs are unique in this all the others, assignment to a single most likely regard. pathway was not possible. Since several different Temporal trends in invasion records are noto- pathways have operated during the same time riously challenging to interpret (Cohen and Carl- period and with the same end points, such as his- ton 1998; Ruiz et al. 2000a; Costello and Solow toric trade ships, modern ballast water, and oys- 2003). Although the difference in fit among lin- ter shipments all arriving from Japan or the east ear, polynomial, and exponential models was coast of North America, it is possible that many slight, their long-term predictions would vary species, particularly benthic invertebrates with substantially. Making future projections clearly pelagic larval stages, have been transported by requires further investigation of the mechanisms several means. underlying these trends. Nevertheless, the recent arrival of relatively conspicuous species such as Temporal trends the European green crab Carcinus maenas and the Asian varnish clam Nuttallia obscurata The number of introduced species in the NEP (Miller 1996; Byers 2002) indicate that in spite of has clearly increased over the last century. We inevitable sampling and detection artifacts the 380 number of invaders in the NEP continues to mercial shipping traffic to Willapa Bay may increase. account for its lower diversity of unique invaders. These regional patterns highlight the impor- tance of invasion pathway type and intensity in Regional differences determining the resulting distribution and com- position of introduced species. At the same time, Regional analysis within the NEP allows further the high proportion of multiple-pathway invaders investigation of the relative roles of different illustrates the importance of considering a range invasion pathways. It is not surprising that the of possible invasion routes for each species. Straits and Sound region, which covers by far Clearly, if we could reconstruct the true invasion the largest area, had the greatest number of pathway of each of these invasions (in the unli- invaders. However, this region had fewer ship- kely case that all these species indeed arrived in ping-mediated invasions than would be predicted only one manner), we would expect the observed from its cumulative shipping traffic volume, distribution of invasion pathways to change whereas the three smaller coastal bays had more. somewhat. Organism retention and subsequent recruitment may be more pronounced in the enclosed coastal Invader impacts bays than in the comparatively open waters of the Straits and Sound, leading to a tighter cou- The ecological and economic impacts of only a pling between invasion and shipping patterns. small number of the 123 established NEP invad- Among the three outer-coast bays, Willapa Bay ers have been studied. Several species act as eco- had the lowest number of invaders and the least system engineers, altering habitat structure and shipping activity. This suggests that across subre- availability (Crooks 2002). The cordgrasses Spar- gions with similar retention, invasion success tina spp., the eelgrass Zostera japonica, and the may correlate better with propagule pressure. marine alga Sargassum muticum all increase habi- In two regions, Straits and Sound and Willapa tat structure complexity, with impacts on native Bay, we found more oyster- than shipping-medi- and introduced estuarine species (Britton-Sim- ated invasions. This result is consistent with our mons 2003; Wonham 2003). S. alterniflora, for expectation that benthic species planted directly example, affects the abundance of epifaunal crus- in the intertidal would have an invasion advan- taceans, infaunal polychaetes, the native clam tage over those dispersed into the water column Macoma balthica, and the introduced clams Mya from ship hulls or ballast water. However, with- arenaria and Venerupis philippinarum (Ratchford out knowing the total number of species and indi- 1995; Zipperer 1996; Dumbauld et al. 1997). viduals released, the invasion success rates Z. japonica negatively affects a native congener associated with each pathway cannot be deter- (Nomme and Harrison 1991a, b; Merrill 1995), mined. For example, the sources, density, and alters decomposition rates (Hahn 2003), and total volume of oysters planted in each bay is tends to increase taxon density and richness for unknown but clearly would have influenced the small infaunal invertebrates while inhibiting lar- propagule pressure of additional hitchhiking spe- ger burrowers and having a wide range of cies delivered to the region. The opposite pattern impacts on epifauna (Harrison 1987; Posey 1988; in Coos Bay, where there were more shipping- Simenstad et al. 1988). than oyster-mediated invasions, may in part The introduced hornsnail Batillaria attramen- reflect its smaller size and greater larval retention. taria provides habitat for native hermit crabs In addition, the comparatively high proportion of Pagurus spp. and introduced shell symbionts multiple-pathway invaders here may indicate a Crepidula convexa and Diadumene lincata, as well more complex invasion history in Coos Bay that as serving as a host for the introduced trematode remains to be investigated. Willapa Bay had the Cercaria batillariae. Batillaria also enhances the fewest unique species records. Although oyster abundance of the introduced mudsnail Nassarius shipments may historically have delivered similar fraterculus, and the introduced eelgrass Z. japon- species to all four regions, the much lower com- ica (O’Connor et al. 2002; Torchin et al. 2004). 381
Trophic interactions have also been reported southwest Pacific (SWP), and northeast and for some invaders. Spartina carbon is found in northwest Atlantic (NEA, NWA). On closer con- tissue of the introduced cumacean Nippoleucon sideration, however, we find that NWP databases hinumnensis, which in turn is eaten by native remain limited to date, that SWP databases Pacific salmon (Lubetkin 1997; S. Simenstad, represent substantially different invasion path- University of Washington School of Aquatic and ways, species, and historical biogeographies, and Fishery Sciences, unpublished data), and Zostera that the waters of the NWA are considerably japonica is consumed by isopods and foraging colder than those of the NEP. The northeast ducks (Thom et al. 1991, Baldwin and Lovvorn Atlantic Ocean thus emerges as the most relevant 1994). The Asian varnish clam Nuttallia obscura- comparison region. Partial data on introduced ta and the copepod Pseudodiaptomus inopinus are marine organisms are available for the NEA, both now abundant prey items for native preda- particularly for the British Isles (Eno 1996; Eno tors, presumably altering trophic relationships et al. 1997). In both NEA and NEP reviews, a and nutrient cycling in their respective habitats potentially very large number of invaders remain (Bollens et al. 2002; Byers 2002). undocumented, especially among smaller and In economic terms, some invaders are impor- lesser-known invertebrate groups such as tant recreational and commercial harvest species sponges, flatworms, hydroids, polychaetes, and (bivalves Crassostrea gigcis, Mya arenaria, Merc- bryozoans. This taxonomic underestimation enaria mercenaria, Venerupis philippinaruni), noted, the most striking differences between the whereas others are considered pests (flatworm NEP and NEA are in the ratio of macroalgal to Pseudostylochus ostreophagus, oyster drills Ocine- invertebrate species (NEP 1 : 32 vs NEA 1 : 2) brellus inornatus and Urosalpinx cinerea, parasites and the overall trend in cumulative invasion Mytilicola orientalis and Pseudomyicola ostreae, records (NEP accelerating vs NEA linear). and shipworm Teredo navalis). Further comparisons within and among ocean Understanding the overall role of the intro- basins will await more detailed data on historical duced biota in this system requires further pathways, sources, habitats, and invasion timing. detailed study of the extent and impacts of many Our ability to predict future invasion patterns more of these species (e.g., Parker et al. 1999). will be much enhanced by the availability of We emphasize that the lack of reports of ecologi- detailed regional analyses that will allow us to cal, environmental, social, or economic impacts extend our approach to a global framework. of the majority of the introduced species treated here does not mean that such impacts do not exist: a lack of study should not be confounded with a lack of impact. Acknowledgements
Interoceanic comparison We are grateful for the generous sharing of taxo- nomic expertise, samples and unpublished Retrospective invasion analyses for distinct bi- records by J. Chapman (amphipods). J. Cordell ogeographic regions such as these have substan- (copepods and insects), K. Graham (mussels), S. tial value. They provide critical insights into the Henderson (bryozoans), T. Klinger (algae), K. Li invasibility of particular habitats and subregions, and C. Staude (amphipods), C. Mills (hydrozo- links to pathway risk analysis, and historical ans), P. Connors and S. Hacker (vascular plants). baseline data against which to compare current This research was conducted with support from ecological changes. These reviews also provide a Graduate Research Fellowship NA77OR0250, necessary foundation to focus specific manage- Estuarine Reserves Division, Office of Ocean and ment practices on both particular pathways and Coastal Management, National Ocean Service, taxa. National Oceanic and Atmospheric Administra- Ideally, we would extend this analysis from a tion (Padilla Bay National Estuarine Research regional to a global scale. Candidate regions for Reserve) to MJW, and the Pew Fellowships in comparison include the northwest Pacific (NWP), Marine Conservation to JTC. Appendix 1. Introduced marine invertebrates and algae established in the Northeast Pacific (Humboldt Bay, California, to the Queen Charlotte Islands, British Columbia). 382 Origin as in Table 1, pathway as in Table 2, regions as in Table 3. Decade refers to first collection if known, otherwise to publication date of first record (in parentheses). The status of certain species has been updated since reviews by Wonham (2000) and Ruiz et al. (2001) range extensions reported in Cohen et al. (2001) are included, but records of species new to the Pacific coast are not. Taxon Origin Pathway Northeast Pacific Regions Decade Source SS WB CB HB Other Invertebrates Foraminiferans Trochammina hadai WP BW/CO/ X X X 1970s McGann et al. (2000) SF Sponges Halichondria bowerbanki WA CO/SF X X X 1970s Carlton (1979), Austin (1985), Cohen and Carlton (1995) Haliclona sp. WA CO/SF X X X 1970s Carlton (1979), Shapiro and Associates (1980), Cohen and Carlton (1995) Microciona prolifera WA CO/SF X X (1960s) Carlton (1979), Cohen and Carlton (1995) Cnidarians Hydrozoans Blackfordia virginica PC? BW/SF X 1990s Mills and Sommer (1995) Cladonema radiatum EA SF? X 1980s Kozloff (1996), C.E. Mills (unpublished data) Cordylophora caspia PCSFXXXXX1920s Carlton (1979), Cohen et al. (2001) Ectopleura (= Tubularia) NA CO/SF X X X (1910s) Monroe (1973), Carlton (1979) crocea Anthozoans Diadumene cincta NA SF X 1980s Carlton (1989) Diadumene leucolena NA CO/SF X X (1960s) Carlton (1979), Boyd et al. (2002) Diadumene lineata WP CO/SF XXXX 1900s Carlton (1979) (=Haliplanella lineata = H. luciae) Platyhelminths Pseudostylochus ostreophagus WP CO X 1950s Carlton (1979) Cercaria batillariae WP CO X 2000s Torchin et al. (in press) Annelids Oligochaetes 1970s Limnodriloides monothecus NA BW/CO X Brinkhurst and Baker (1979) Paranais frici PC BW/CO X (1970s) Brinkhurst and Coates (1985) Tubificoides brownae NA BW/CO X X 1970s Brinkhurst (1986) Tubificoides diazi NA BW/CO X X 1970s Brinkhurst (1986) Tubificoides wasselli NA BW/CO X 1970s Brinkhurst (1986) Polychaetes Heteromastus filiformis WA BW/CO X X X X 1960s Carlton (1979), Cohen and Carlton (1995), Boyd et al. (2002) Hobsonia florida WA CO X X X 1940s Banse (1979), Cohen et al. (2001) Neanthes (=Nereis) succinea NA CO/SF X X X 1970s Carlton (1979), Cohen and Carlton (1995), Cohen et al. (1998) Polydora cornuta (=ligni) NA CO/SF XXXXX1930s Boyd (1975), Hancock et al. (1977), Carlton (1979), Cohen et al. (2001) Pseudopolydora kempi WP BW/CO/SF XXXXX1950s Boyd (1975), Hancock et al. (1977), Carlton (1979), Cohen et al. (2001) Pseudopolydora paucibranchiata WP BW/CO/SF X X X X 1970s Carlton (1979), Boyd et al. (2002) Sabaco elongatus WA BW/CO X 1990s F. Cole, Environmental Protection Agency, pers. comm. to JTC (2000) Streblospio benedicti WA CO/SF XXXXX1970s Boyd (1975), Hancock et al. (1977), Carlton (1979), Cohen et al. (2001) Molluscs Gastropods Batillaria attramentaria WP CO X 1920s Carlton (1979) (=B. zonalis = B. cumingi) Cecina manchurica WP CO X X 1960s Carlton (1979) Crepidula convexa WA CO X 1990s Carlton (1992) Crepidula fornicata WA CO X X X X 1900s Carlton (1979, 1992) Crepidula plana WA CO X X 1930s Carlton (1979, 1992) Ilyanassa obsoleta WA CO X X 1940s Carlton (1979) Myosotella (=Ovatella) myosotis EA CO/SF XXXXX1870s Carlton (1979) Nassarius fraterculus WP CO X 1960s Carlton (1979) Ocinebrellus inornatus WP CO X X X X 1920s Carlton (1979, 1992), (=Ceratostoma inornatum Shapiro and Associates (1980) =Ocenebrajaponica) Philine auriformis SH BW X 1990s F. Goddard, pers. comm. to JTC (1998) Potamopyrgus antipodarum SH CM X 1990s Systma et al. (2002) Tenellia adspersa NA BW/CO/SF X 1970s Hancock et al. (1977) Urosalpinx cinerea WA CO X X X 1920s Carlton (1979, 1992) Bivalves Corbicula fluminea WP IP X 1930s Carlton (1979) (=C. manilensis) Crassostrea gigas WPCOXXXX 1910s Monroe (1973), Carlton (1979, 2000) Crassostrea virginica WA CO X 1915s Carlton (1979, 1992) 383 Appendix 1. Continued. 384 Taxon Origin Pathway Northeast Pacific Regions Decade Source SS WB CB HB Other Gemma gemma WA CO X 1940s Shapiro and Associates (1980), T. Miller pers. comm. to JTC (1999) Laternula marilina WP BW/CO X X 1990s Miller et al. (1999) Lyrodus takanosimensis WP CO X 1980s Carlton (1992) Mercenaria mercenaria WA CO/IP X X (1970s) Monroe (1973), Coan et al. (2000) Musculista (=Musculus) senhousia WP CO X 1950s Carlton (1979) Mya arenaria WACO/IPXXXXX1880s Carlton (1979), Shapiro and Associates (1980) Neotrapezium (=Trapezium) liratum WP BW/CO X X (1940s) Carlton (1979), Cohen et al. (2001) Nuttallia obscurata WP BW X X 1990s Byers (2002) Petricolaria (=Petricola) WA CO X 1940s Carlton (1979) pholadiformis Teredo navalis UNK SF X X X 1950s Carlton (1979) Venerupis philippinarum WP CO X X X X 1930s Carlton (1979, 1992) (=Tapes japonica) Arthropods Crustaceans Copepods Acartiella sinensis WP BW X 1990s J. Cordell (pers. comm. 1999) Limnoithona (=Oithona) WP BW X 1990s J. Cordell (pers. comm. 1999) sinensis Paramisophria sp. WP BW X 1990s J. Cordell (pers. comm. 1999) Pseudodiaptomus inopinus WP BW X X X X 1990s Cordell and Morrison (1996), Cordell (1998) Pseudodiaptomus marinus WP BW X 1990s J. Cordell (pers. comm. 1999) Pseudomyicola ostreae WP CO X X X X 1930s Carlton (1979) (=Mytilicola ostreae, M. orientalis) Sinocalanus doerrii WP BW X 1990s J. Cordell (pers. comm. 1999) Barnacles Balanus improvisus NA CO/SF X X X X 1950s Carlton (1979) Cumaceans Nippoleucon WP BW/CO X X X X 1970s Hancock et al. (1977), Cohen and (=Hemileucon) hinumensis Carlton (1995), Cohen et al. (1998, 2001) Tanaids Sinelobus stanfordi UNK BW/CO/ X X X 1970s Levings and Rafi (1978), Cohen and SF Carlton (1995) Isopods Iais californica SH SF X X 1930s Carlton (1979, 2000) Limnoria quadripunctata UNK SF X X 1940s Carlton (1979) Limnoria tripunctata UNKCO/SFXXXXX1960s Carlton (1979), Shapiro and Associates (1980), Barnhardt et al. (1992), Carlton and Hodder (1995) Sphaeroma quoyanum SH SF X X 1930s Carlton (1979), Cohen and Carlton (1995) Synidotea laevidorsalis WP BW/CO/SF X 1980s Chapman and Carlton (1991) Amphipods Ampithoe valida WA BW/CO/SF X X X X 1950s Carlton (1979), Conlan and Bousfield (1982), Cohen and Carlton (1995), Cohen et al. (2001) Caprella mutica WP BW/CO/SF X X X 1970s Carlton (1979 (as C. acanthogaster), 2000); Cohen et al. (1998) Chelura terebrans UNK SF X X 1950s Carlton (1979), Boyd et al. (2002) Monocorophium NA BW/CO/SF X X X X X 1910s Carlton (1979), Cohen et al. (2001) (=Corophium) acherusicum Monocorophium NA BW/CO/SF X X X X 1910s Carlton (1979, 2000) Cohen et al. (=Corophium) insidiosum (2001) Eochilidium sp. WP BW X 1990s C. Staude and K. Li (pers. comm.), Cohen et al. (2001) Grandidierella japonica WP BW/CO X X X X 1970s Cohen and Carlton (1995); Cohen et al. (1998); J. Chapman, pers. comm. to JTC (1997) Incisocalliope WP SF X X X X 1980s Chapman (1988), Carlton (2000), (=Parapleustes) derzhavini Cohen et al. (2001), Boyd et al. (2002) Jassa marmorata (=J. falcata) WA BW/CO/SF X X X X X 1940s Carlton (1979), Conlan (1990), Bott and Diebel (1982), Cohen et al. (2001) Melita nitida WA BW/CO/SF X X X X X 1950s Carlton (1979), Cohen and Carlton (1995), Jarrett and Bousfield (1996), Cohen et al. (2001), Boyd et al. (2002) Microdeutopus gryllotalpa WA BW? X 1990s J. Chapman and T. Miller, pers. comm. to JTC (2000) Paracorophium sp. SH BW X 1990s J. Chapman and T. Miller, pers. comm. to JTC (2000) Decapods Carcinus maenas WA CM X 1990s Miller (1996) Exopalaemon modestus WP BW X 1990s Emmett et al. (2002) Palaemon macrodactylus WP BW X X 1970s Cohen and Carlton (1995), Carlton (2000) Rhithropanopeus harrisii WA BW/CO/SF X X 1950s Carlton (1979) Insects Clunio tsushimensis WP BW/SF X 1980s J. Cordell, pers. comm. to JTC (2000) Kamptozoans Barentsia benedeni NA BW/CO X X X 1980s Carlton (1989), Wasson (1997), Boyd et al. (2002) 385 Appendix 1. Continued. 386 Taxon Origin Pathway Northeast Pacific Regions Decade Source SS WB CB HB Other Bryozoans Bowerbankia ‘gracilis’ UNK CO/SF X X X X 1920s O’Donoghue and O’Donoghue (1923a, b), Cohen et al. (2001), Barnhardt et al. (1992) Bugula neritina UNK CO/SF X X 1980s Carlton and Hodder (1995), Cohen and Carlton (1995), Carlton (2000) Bugula stolonifera UNK SF X 1990s Cohen et al. (1998) Conopeum tenuissimum WA CO/SF X 1970s Carlton (1989) Cryptosula pallasiana UNK CO/SF X X X X 1960s Carlton (1979), Hewitt (1993), Boyd et al. (2002) Schizoporella unicornis WP CO/SF X X X X X 1920s Carlton (1979, 1989), Barnhardt et al. (1992) Triticella sp. WP? BW X 1980s Hewitt (1993) Watersipora ‘subtorquata’ WP BW/SF X X 1990s Hewitt (1993), Boyd et al. (2002) Urochordates Ascidians Botrylloides violaceus WP CO/SF X X X X 1970s Carlton (1979 (as Botrylloides sp.), (=B. aurantius) 2000), JTC (pers. obs.) Botryllus schlosseri NA CO/SF X X X X X 1970s Carlton (1979, 2000), Cohen et al. (1998), JTC (pers. obs.) Boyd et al. (2002) Ciona savignyi WP BW/SF X X 1990s Cohen et al. (1998), Boyd et al. (2002) Molgula manhattensis NA BW/CO/ X X X X 1970s Carlton (1979), Cohen and Carlton SF (1995), Cohen et al. (1998), Boyd et al. (2002) Styela clava WP BW/SF X X X 1990s Cohen and Carlton (1995), Cohen et al. (1998), Boyd et al. (2002) Macroalgae Rhodophytes Gelidium vagum WP CO X 1980s Renfrew et al. (1989) Lomentaria hakodatensis WP CO X X 1960s Hawkes and Scagel (1986), Boyd et al. (2002) Phaeophytes Sargassum muticum WP CO X X X X X 1940s Scagel (1956), Cohen et al. (2001)
Diatoms Attheya (=Gonioceros SH BW? X Lewin and Norris (1970) =Chaetoceros) armatus Appendix 2. Introduced marine and maritime plants, and marine and estuarine fishes established in the Northeast Pacific (Humboldt Bay, California, to the Queen Char- lotte Islands, British Columbia). Origin as in Table 1, pathway as in Table 2. Records listed here for provinces and states, not for NEP subregions (BC, British Columbia; WA, Washington; OR, Oregon; CA, California north of Cape Mendocino). Decade refers to first collection if known, otherwise to publication date of first record (in par- entheses). The relative paucity of data for maritime plant pathways and dates presumably reflects early inadvertent introductions for many of these species. Taxon Origin Pathway Northeast Pacific records Decade Source BC WA OR CA Marine vascular plants Poaceae Spartina alterniflora WA IP, CO?/ X X X 1940s Aberle (l993), Frenkel (1987) SF? Spartina anglica EA IP X X 1960s Aberle (1993) Spartina densiflora SH DB X 1920s Saint-Yves (1932), F. Jacquemoud, pers. comm. to MJW (2003), Boyd et al. (2002) Spartina patens WA CO X 1960s Aberle (1993), Frenkel and Boss (1988) Zostera japonica WP CO X X X 1950s Harrison (1987), Bigley and Harrison (1982) Maritime vascular plants Brassicaceae Cakile edentula EA Unk X X X X Unk Hickman (1993), Cooke (1997) Cakile maritima EA Unk X X X X Unk Calder and Taylor (1968), Hickman (1993) Asteraceae Cotula coronopifolia SH DB X X X X Unk Calder and Taylor (1968), Hickman (1993), Cooke (1997) Graminae Parapholis incurva EA Unk X X X Unk Hickman (1993), Munz (1959), Barnhardt et al. (1992), USDA (2002) Parapholis strigosa EA Unk X Unk Barnhardt et al. (1992) Plantaginaceae Plantago coronopus EA Unk X X X X Unk Munz (1959), Hickman (1993), Qian and Klinka (1998), USDA (2002) Caryophyllaceae Spergularia bocconii EA Unk X Unk Hickman (1993) Spergularia maritima EA Unk X X Unk Munz (1959), Hickman (1993) (=S. media (L.) K. Presl. ex Griseb.) Aizoaceae Tetragonia tetragonoides SH IP X X Unk Hickman (1993) Marine and estuarine fishes Clupeidae Alosa sapidissima (American shad) WA IP X X X X 1870s–80s Smith (1896), Fuller et al. (1999) Dorosoma petenense (threadfin shad) WA IP X (1950s) Fuller et al. (1999) Poeciliidae Gambusia affinis (Western mosquitofish) WA IP X X X Unk Fuller et al. (1999) 387 388
Appendix 2. Continued. Taxon Origin Pathway Northeast Pacific records Decade Source BC WA OR CA Lucania parva (rainwater killifish) WA BW; IP X 1950s Fuller et al. (1999) Moronidae Morone saxatilis (striped bass) WA IP X X X X 1900s Fuller et al. (1999)
Salmonidae Salmo trutta (brown trout) WA IP X X X 1920s Fuller et al. (1999) 389
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