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1
MANAGING MULTIPLE VECTORS for MARINE INVASIONS in an 1
INCREASINGLY CONNECTED WORLD 2
3
Susan L. Williams1,2* 4
Ian C. Davidson3,4 5
Jae R. Pasari1 6
Gail V. Ashton5 7
James T. Carlton6 8
R. Eliot Crafton7 9
Rachel E. Fontana1,7,8 10
Edwin D. Grosholz9 11
A. Whitman Miller4 12
Gregory M. Ruiz4 13
Chela J. Zabin5,9 14
15
1Bodega Marine Laboratory, University of California-Davis, PO Box 247, Bodega Bay, 16
CA 94923-0247,*([email protected]); 2Department of Evolution and Ecology, 17
University of California-Davis, Davis, CA 95616; 3Environmental Sciences and 18
Management, Portland State University, Portland, OR; 4Smithsonian Environmental 19
Research Center, PO Box 28, Edgewater, MD 21037-0028; 5Smithsonian Environmental 20
Research Center, 3152 Paradise Dr., Tiburon, CA 94920; 6Maritime Studies Program, 21
Williams College and Mystic Seaport, PO Box 6000, Mystic, CT 06355-0990; 7Graduate 22
Group in Ecology, University of California-Davis, Davis, CA 95616; 8Current address: 23
2
Office of Oceanic and Atmospheric Research, National Oceanic and Atmospheric 24
Administration, Silver Spring, MD 20910; 9Department of Environmental Science and 25
Policy, University of California-Davis, Davis, CA 95616. 26
27
Keywords: invasive species, marine, vectors, propagule supply, management 28
29
Susan Williams, PhD, is a professor and coastal marine ecologist who studies the 30
ecological effects of non-native species and applies results to management and policy. 31
Ian Davidson, PhD, is a Research Associate at the Aquatic Bioinvasion Research and 32
Policy Institute. He is a benthic ecologist who focuses on marine invasive species, 33
especially associated with vessels, and applies results to management and policy. 34
Jae Pasari, PhD, teaches and conducts research on ecological invasions in California's 35
marine and terrestrial environments. 36
Gail Ashton, PhD, is a marine ecologist specializing in invasive species. 37
James Carlton, PhD, is a professor and marine biologist at Williams College and director 38
of the Williams-Mystic Maritime Studies Program. His research focuses on marine 39
invasions and extinctions. 40
R. Eliot Crafton is a PhD candidate modeling invasion risk for coastal marine and 41
estuarine species. 42
Rachel Fontana, PhD, is an environmental oceanographer and a National Sea Grant 43
Knauss Marine Policy Fellow in Washington, D.C. 44
Edwin Grosholz, PhD, is a professor and benthic marine ecologist who works on the 45
science and management of biological invasions and coastal restoration. 46
3
A. Whitman Miller, PhD, is a Research Scientist who studies marine and estuarine 47
invasions ecology with a strong focus on the role of commercial ships in the 48
worldwide spread of invasive species. 49
Gregory Ruiz, PhD, is a Senior Scientist and head of the Smithsonian Environmental 50
Research Center’s Marine Invasion Research Laboratory. He applies invasive species 51
research results to management and policy. 52
Chela Zabin, PhD, is a marine ecologist interested in native species restoration and 53
management of invasive species. 54
55 56
4
Abstract 57
Invasive species remain a major environmental problem in the world's oceans. Managing 58
the vectors of introduction is the most effective means to mitigate this problem, yet 59
current risk assessments and management strategies largely focus on species, not vectors, 60
and certainly not multiple vectors acting simultaneously. To highlight the issue that 61
multiple vectors are contributing to invasions, we analyzed the historical and potential 62
contemporary contributions of eight maritime vectors to the establishment of non-63
indigenous species in California, where most species were associated with two to six 64
vectors. Vessel biofouling looms larger than ballast water as a major vector and a 65
management opportunity but aquaculture risk appears reduced from historic 66
contributions. Standardized data on species abundances in each vector are lacking for a 67
robust cross-vector assessment, which could be obtained in a proof of concept ‘vector 68
blitz’. Management must shift away from one or two target vectors to coordination across 69
multiple vectors. 70
71
72
5
Non-indigenous species (NIS) are widespread throughout Earth’s oceans and coasts, 73
where they cause environmental impacts and economic damages (Carlton 1999). They 74
have been associated with declines in marine populations (Kappel 2005), alteration of 75
food webs (Nichols et al. 1990, Oguz et al. 2008), habitat modifications that affect 76
community structure and function (Neira et al. 2006, Sousa et al. 2009), and delivery of 77
toxic microorganisms of concern for sea life and human health (Ruiz et al. 2000). 78
79
Multiple vectors operating in an increasingly connected world 80
Increasing global trade, novel trade routes, climate change, habitat modification, 81
fisheries, and invasions themselves can combine to create increasing opportunities for 82
introductions of marine NIS. Global trade increased dramatically in the latter half of the 83
20th Century, driven by human population growth, changes in policies, and increased 84
efficiency in shipping (Hulme 2009). Previously remote locales such as Antarctica, where 85
many marine species are endemic, have come under increasing risk from NIS 86
introductions (Smith et al. 2012). At the opposite pole, the Northwest Passage has been 87
sufficiently ice-free for navigation since the summer of 2007, shortening the path 88
between the Atlantic and Pacific oceans and increasing opportunities for human-mediated 89
species introductions (Niimi 2004). As oceans warm, NIS can gain a foothold over native 90
marine species (Sorte et al. 2010). New conservation strategies such as “assisted 91
colonization” or “managed relocation” further promote transfers of species beyond their 92
native ranges (Schwartz et al. 2012). 93
94
95
6
One by one- single species, single vector risk assessments 96
In this increasingly connected world, the most effective means to reduce future ecological 97
and economic costs of NIS is to prevent their introductions by managing the vectors that 98
deliver them, rather than focusing efforts on the management of individual species or 99
even individual vectors (Ruiz and Carlton 2003, Reaser et al. 2008). Despite this widely 100
accepted recommendation, most research and management tackles the problem of 101
biological invasions on a species-by-species and vector-by-vector approach. 102
103
Species approaches have included “black listing” based on evidence that a species could 104
be or is an injurious pest. This approach is usually based on previously-identified bad 105
actors and it is laborious, being impractical for the large number of species that circulate 106
in multiple vectors and especially those without an invasion history (Simberloff 2006, 107
Reaser et al. 2008). A formal risk assessment, involving evaluation of the probability that 108
a species will be introduced, establish, and cause ecological or economic harm, requires 109
both more data and effort than is available for most species. 110
111
Various types of NIS risk assessments are being considered or applied by management 112
authorities from states to nations (Kolar 2004, Gordon et al. 2012). Some assessments 113
favor matching environmental conditions of native and non-native ranges to predict risk, 114
some take a spatially-explicit landscape approach to identify sites that are vulnerable to 115
invasions, some include management actions, and others focus on propagule pressure or 116
address how the recipient community can shape the success or failure following an 117
introduction. NIS risk assessment makes economic sense (Keller et al. 2007, Springborn 118
7
2011) and has made substantial progress over the past decade, but it is still based 119
primarily on the risk posed by specific species or species characteristics related to 120
invasiveness (Hayes 2002, Hayes and Sliwa 2002, Orr 2003, Keller et al. 2007, Campbell 121
2009, see Leung et al. 2012 for theoretical framework). 122
123
In this article, we highlight the challenge that multiple vectors pose in evaluation and 124
management of invasions, using marine and estuarine (hereafter ‘marine’) NIS as a 125
model. Maritime vectors are diverse. Major vectors include: 1) ballast water, which is 126
already the subject of management to varying degrees (Miller et al. 2011), 2) ‘biofouling’ 127
of large and small vessels by a community of sessile and associated mobile organisms 128
that colonize and grow on any wetted surface of a vessel, such as hulls, anchors, storage 129
lockers, or other colonizable locations (Mineur et al. 2008, Davidson et al. 2009, Wanless 130
et al. 2010), 3) aquaculture (Naylor et al. 2001), 4) live seafood (Chapman et al. 2003), 5) 131
live bait (Kilian et al. 2012), 6) ornamental species trade (Rhyne et al. 2012), and 7) 132
marine debris (Barnes 2002). Maritime vectors are also temporally dynamic, with both 133
gradual and punctuated changes, the latter demonstrated by biofouled debris from the 134
2011 Japanese earthquake and tsunami that washed ashore in North America. The 135
tsunami debris instigated a rapid management response [25 June 2013; 136
www.anstaskforce.gov/Tsunami/FINAL%20JTMD%20Biofouling%20Response%20Prot137
ocol_19%20Oct%202012.pdf], which is crucial to preventing introductions, but also 138
highlighted the ad hoc manner in which limited management and scientific resources are 139
allocated among multiple vectors when no decision has been made about vector 140
8
prioritization. Our analysis of maritime vectors helps explain why it is difficult to 141
prioritize among vectors. 142
143
The plethora of existing vectors and temporal changes in operation is not generally 144
recognized, except by the scientists who study them. It is safe to say that the broader 145
public, the media, and the environmental, management and political communities are 146
largely unaware of how little is known about these vectors in space and time. For 147
example, the education campaigns that raised public awareness about ballast water as a 148
possible vector for invasive species contrasts sharply with the lack of awareness about 149
cultured non-native oysters that have become feral and can dramatically change marine 150
environments (Ruesink et al. 2005). In a different example, the public is not likely to 151
know that over 100,000 individuals of the quagga mussel (Dreissena rostriformis 152
bugensis), over 100 sharks, and transgenic tilapia and salmon, all of which are restricted 153
species in California, were permitted for importation in 2009, for research, exhibition 154
including at public zoos and aquariums, or aquaculture (see below for data sources). Only 155
recently have research facilities and public zoos and aquariums taken steps to prevent the 156
release of NIS. The general incognizance of vector multiplicity is evident in regulatory 157
frameworks based on single species or vectors. For instance, the Lacey Act administered 158
by the US Fish and Wildlife Service (USFWS) regulates injurious pests species-by-159
species and the International Maritime Organization is advancing ballast water 160
management. The value of these frameworks cannot be discounted, but they do not 161
address the issue of managing multiple vectors. 162
163
9
How close are we to reliably comparing the relative risk of different maritime vectors or 164
their cumulative risk? Which among the many operating vectors offer management 165
opportunities or merit prioritization under the limited available resources? The relative 166
importance of maritime vectors has been assessed most often by tallying the number of 167
species attributed to vectors that are often defined in different ways (Bax et al. 2003, Ruiz 168
et al. 2011), an approach also applied to freshwater and terrestrial NIS vectors (e.g., 169
Keller et al. 2009). Although these studies have advanced the management of marine 170
invasive species, they are largely retrospective analyses. A few quantitative risk 171
assessments for single marine species have been accomplished (e.g., Herborg et al. 2007, 172
2009, Thierrault and Herborg 2008). A few other studies have undertaken a vector-based 173
risk assessment by obtaining abundances of NIS in invasive pathways (Hayes 2002, 174
Hayes and Sliwa 2002, Barry et al. 2008, Acosta and Forrest 2009). Hayes (2002) used 175
shipping records and species distributions to estimate invasion potential, added a web-176
based questionnaire to assess economic, ecological, and health impacts for potential 177
marine invaders in New Zealand, and estimated uncertainty using interval arithmetic. 178
Single-vector management is certainly an improvement over single-species management, 179
but might not substantially reduce invasions if many other vectors are in place. To our 180
knowledge, there has been no attempt to quantify the relative or combined risk that 181
multiple maritime vectors pose, beyond vector attribution tallies, or to evaluate their past, 182
present and future changes. 183
184
To illustrate both the need for and the challenge of assessing the risk posed by multiple 185
vectors, we compared available data for eight maritime vectors operating in California: 186
10
commercial vessel ballast water, commercial vessel biofouling, recreational vessel 187
biofouling, fishing vessel biofouling, aquaculture, and trades in ornamental species, live 188
seafood, and live bait. California provides a good model to illustrate the state of 189
knowledge of multiple vectors for several reasons. California is a major introduction 190
point for marine NIS and serves as a nexus for their establishment and spread. 191
Furthermore, the state supports a relatively high level of activity across diverse vectors 192
(Ruiz et al. 2011). Its large marine economy (Kildow and Colgan 2009) has already been 193
taxed by marine invasive species (Anderson 2005, Fernandez 2008), which helped spur 194
state government’s interest in a multiple-vector management approach. The vectors 195
considered here operate globally; therefore, their comparison should provide a useful 196
generalized illustration of the issue of multiple vectors. 197
198
Multiple vectors characterize California’s historical marine invasions 199
Data often limit quantitative NIS risk assessment (Gertzen and Leung 2011, Leung et al. 200
2012). The most readily available data are NIS lists that provide information on the 201
species, introduced locales, and dates of first record (e.g., National Exotic Marine and 202
Estuarine Species Information System [NEMESIS, 3 July 2013; 203
http://invasions.si.edu/nemesis/index.html]; National Introduced Marine Pest Information 204
System [NIMPIS, 16 June 2013; www.marinepests.gov.au/nimpis]). We analyzed 205
California’s marine NIS invasion history based on a subset of data from NEMESIS 206
(accessed 18 March 2013) for all non-freshwater, non-native invertebrates (except 207
insects) and algae known to have established in California from 1853-2011. These taxa 208
include the vast majority of marine NIS in California. We updated the study by Ruiz et al. 209
11
(2011) on vector attribution to individual species and expanded it to include multiple 210
introduction events by including the dates and specific bays of introduction within the 211
state, allowing finer parsing of vector attribution. We identified that at least 235 NIS have 212
established in California’s marine and estuarine waters (Supplemental Material, Table A), 213
including two species that were subsequently eradicated (the seaweed Caulerpa taxifolia, 214
and the polychaete worm Terebrasabella heterouncinata). 215
216
We then addressed vector strength (the number of invasions attributed to a vector, Ruiz 217
and Carlton 2003) in several ways. Based on life history traits, timing, and location of 218
NIS detections and vector operations (see Ruiz et al. 2011 for description), 90 of the 235 219
species were classified as introduced to California almost certainly by only a single 220
vector (figure 1a; Supplemental Material, Table A). The single-vector species provided 221
the most conservative estimate of the historical strength of each vector. For these single-222
vector species, although ballast water was a major vector, non-ballast water vectors 223
together accounted for more than twice the number of established NIS in comparison to 224
ballast water alone. Furthermore, vessel biofouling was identified as the vector for as 225
many established NIS as ballast water and aquaculture combined. 226
227
The other 145 NIS (61% of the total) were attributed to between two and six possible 228
vectors. For these, we summarized vector strength in two ways. First, for each species, 229
we summed the number of establishment events (non-transient presence of a species in a 230
bay) attributed to each possible vector. For example, if a multiple-vector species was 231
known from nine different bays and ballast was a sole or possible vector for three of these 232
12
bays, three invasion events were attributed to ballast for that species. This approach 233
identifies the maximum number of establishment events per vector. Second, we weighted 234
vectors proportionately by the number of events attributed to each for each individual 235
species. When more than one vector was plausible for the presence of a species in a bay, 236
it was treated as multiple events, each by a single vector. For example, if a species was 237
known from 10 bays, including three associated with ballast alone, two with ballast and 238
vessel biofouling together, and five with aquaculture only, ballast was weighted as 0.42 239
(5/12). Thus, each species is weighted equally (as 1.0), regardless of number of invasion 240
events, and each plausible vector per introduction event has equal probability in its 241
proportional contribution. 242
243
For these multiple-vector species, our unweighted estimate of possible vector importance 244
indicated that ballast and vessel biofouling were the most common vectors involved 245
(figure 1b). Of the 77 species introduced by two vectors, 49% were attributed to ballast 246
water and vessel biofouling, 26% to aquaculture and vessel biofouling, and 8% to ballast 247
water and aquaculture. Our weighted estimate highlights patterns that are not apparent 248
from the previous, more traditional unweighted analysis alone. While the unweighted 249
analysis demonstrates the magnitude of possible vector importance (for all invasion 250
events), the weighted analysis is informative for generating hypotheses about probable 251
vector importance on a per species basis. For example, the unweighted estimate indicates 252
aquaculture was a potent possible vector, but the weighted estimate de-emphasized its 253
vector strength relative to ballast water and vessel biofouling (figure 1c). To a lesser 254
13
degree the same can be said of ballast water, whereby its strength is reduced in the 255
weighted estimate compared to vessel biofouling. 256
257
Although the historical data provided some new insights into the relative contributions of 258
vectors introducing marine NIS to California, there are some obvious limitations for a 259
robust comparison of vectors and their relative risk. First, the numbers of species on lists 260
of introduced species such as NEMESIS and NIMPIS are undoubtedly underestimated 261
(Carlton 2009). Second, a more serious limitation is that historical data do not necessarily 262
match the species currently circulating in vectors today and rarely provide information on 263
species abundances. Third, the nature of individual vectors themselves can change over 264
time, both in magnitude and the per-capita transfer of organisms (see below). We thus 265
considered contemporary fluxes of marine NIS to California. 266
267
Contemporary fluxes of marine NIS to California 268
Information on the abundance of organisms circulating in vectors is critical because 269
abundance is highly correlated to the probability of an introduction (Ruiz et al. 2000, 270
Colautti et al. 2006, Hayes and Barry 2008). For risk assessment, ideally both the number 271
of individuals released in a single event (‘propagule size’) and the number of discrete 272
release events (‘propagule number’) would be estimated for each species (Colautti et al. 273
2006). Although ballast water discharge events are recorded in countries including the 274
US, data on release rates for biofoulers, marine ornamentals, seafood and bait are not 275
available (Weigle et al. 2005). Thus, we focused on propagule flux as the numbers of 276
species and individuals circulating in a vector per unit time (standardized to one year). 277
14
278
To investigate propagule flux we mined published data, federal and state records, and 279
conducted field observations (vessel biofouling, air cargo). Flux estimates for recreational 280
vessel biofouling were obtained from: 1) Last Port of Call (‘LPOC’) records of the US 281
Customs and Border Protection (CBP) for small vessel arrivals to California in 2009, and 282
2) sampling hulls of 49 transient vessels between 2010-2011 for species identification 283
and abundances. The flux of NIS through commercial fishing biofouling was estimated 284
from numbers of arrivals to California in 2008, provided by the Pacific Fisheries 285
Information Network [PacFIN, 1 March 2012; www.psmfc.org/program/pacific-fisheries-286
information-network-pacfin]. Flux estimates for commercial vessel biofouling and ballast 287
water discharge were derived from hull surveys of 23 vessels during 2009-2011, the 288
National Ballast Information Clearinghouse [NBIC, 30 January 2013; 289
http://invasions.si.edu/nbic/search.html] arrival and discharge data, and using the mid-290
point of zooplankton concentrations in ballast arriving to the US (Minton et al. 2005). 291
Ornamental species fluxes were estimated from: 1) USFWS’s Law Enforcement 292
Management Information System (LEMIS) records for live marine fish and invertebrate 293
(excluding scleractinian corals) importations into San Francisco and Los Angeles in 2009 294
(the most recent year of complete records) and observations of air cargo inspections in 295
2012, and 2) California Department of Fish and Game (CDFG) permits for restricted 296
species from 1988 through 4 August 2011. We assessed the flux in aquaculture starting 297
with CDFG records, which led to other sources (see below for details). 298
299
300
15
No common currency to compare propagule flux across vectors 301
At present, no single source of NIS information exists for any of these vectors. Also 302
lacking is a common currency to estimate the flux (numbers of individuals and their 303
identity) circulating annually in each vector, except as order of magnitude bounds (figure 304
2). We first identified a specific unit of NIS delivery for biofouling (vessels arriving), 305
ballast water (vessels discharging), and ornamental species (shipments), but aquaculture 306
import permits did not yield a useful unit of delivery (figure 2a). Next, the quantities of 307
organisms associated with each unit of delivery were estimated for recreational and 308
commercial vessels and the ornamental vector. Good records exist for volumes of ballast 309
water discharged, but numbers of organisms in ballast water had to be extrapolated from 310
another study (Minton et al. 2005). Vessel biofouling has been measured variously as the 311
number of macroinvertebrate species in a biofouling community per vessel, the percent 312
cover of biofouling in areas sampled on vessels, or the biomass of fouling per unit area 313
(Davidson et al. 2009). For the ornamental species, LEMIS import permit records provide 314
more indirect but readily available data than for biofouling. Although quantities of 315
ornamental species in the LEMIS records are not always standardized to individual 316
organisms and records do not account for subsequent transfers out of the state, they are 317
probably close to actual quantities. Quantities could not be estimated for fishing vessels 318
or aquaculture (figure 2b) because sampling access has been restricted to extremely few 319
vessels to date and the numbers of organisms listed on aquaculture permits lacked 320
sufficient standardization and specificity to derive quantities (see below). 321
322
16
Moreover, comparisons of measures of species richness are also problematic, having 323
different approaches depending on the vector (figure 3c; see below). Taxonomic 324
identification is best for the aquaculture vector in California, where permitted organisms 325
are identified to the species level without exception. Species composition is problematic 326
in live organism trades (Rhyne et al. 2012, Smith et al. 2012) but still far better than for 327
most ballast water discharges, for which species composition is unknown. USFWS 328
importation records concern only animals, the majority of which fall into generic 329
taxonomic categories (“marine tropical fishes”, “crustaceans”). Plants fall under the 330
jurisdiction of the US Department of Agriculture, where the same issues apply regarding 331
labeling and transfers upon arrival into the country. Marine plants in general are mostly 332
unidentified when observed and under-represented in vector sampling. 333
334
Small recreational and fishing vessels illustrate the fragmented nature of the data (table 335
1). There were 1182 recreational vessels of foreign origin that entered California and 336
registered with CBP in 2009. This number is the same order of magnitude as commercial 337
vessels (1822 reported in NBIC), yet the actual arrivals of recreational vessels in 338
California and their intra-state movements are unknown but certainly higher than the 339
number of foreign vessels that reported to CBP. CBP records include only the initial 340
arrivals in California of vessels with a LPOC outside of the US. Such boats might travel 341
to additional ports where further registration is not required yet NIS might be transferred. 342
Similarly, vessel arrivals from other US states - either US vessels or foreign vessels that 343
reported to CBP upon first arrival in a different state – are not captured by CBP’s 344
California records. We also conducted surveys of certain marinas in the state, which 345
17
revealed that not all foreign arrivals were captured in the records. Fishing vessel data 346
came from a different source (see above), were restricted to where catch was landed (and 347
excluding other movements where fish were not landed), and included only vessels 348
reporting to Washington, Oregon, and California. If a fishing vessel travels outside of 349
these states, non-comparable CBP records should capture foreign voyages but there is no 350
mechanism to capture voyages to other US states. 351
352
Aquaculture provides an example of both the lack of a common currency for 353
contemporary fluxes and also the fragmented nature of the information (figure 3). We 354
initially expected that the NIS flux in aquaculture could be estimated given that the 355
organisms are intentionally imported or outplanted. We began assessing aquaculture NIS 356
fluxes based on CDFG importation and private stocking permits from 1950 through 2011, 357
only to realize that the records were incomplete and highly dispersed across multiple 358
agencies that regulate various aspects of the industry in California. Different sectors of 359
CDFG are responsible for import permits, private stocking permits, aquaculture 360
inspection and planting certificates, and bottom lease records (“proof of use” reports for 361
state-registered aquaculture facilities). Commercial aquaculture facilities, which must be 362
registered with CDFG, must also file a management plan with the California Department 363
of Public Health, a step we recognized only at the end of the data collection period. While 364
these plans indicate potentially farmed acreage, they do not provide information on 365
number of individuals outplanted or even number of acres actually farmed. The US Army 366
Corps of Engineers (ACE) requires permits for aquaculture businesses placing structures 367
that change the flow of water and/or affect the substratum in state or federal waters. We 368
18
examined ACE records held in the Los Angeles office through a Freedom of Information 369
Act request, but the records provided no relevant information on NIS fluxes (records held 370
in the San Francisco office were not readily retrievable). For aquaculture species 371
imported from other countries, USFWS's LEMIS recorded no importations of 372
invertebrate species for aquaculture between 2003-2011. 373
374
Even taken together, these numerous types of records for California marine aquaculture 375
provided little information on NIS fluxes. Abundances were reported as cases, bushels or 376
thousands of seed individuals. Although California aquaculture import permits must list 377
the intended species and exporter location, there is no post-permit requirement to report 378
the volume or number actually imported. Aquaculture “proof of use” reports specify the 379
number of plantings for a subset of aquaculture facilities (figure 3), but listing the source 380
is voluntary. To further complicate the issue, aquaculture leases were managed variously 381
by CDFG, conservation districts, cities, and a private energy-generating company. The 382
complexity of the aquaculture regulatory framework is challenging for both the industry 383
and the regulators and is a cogent example of the long-recognized need for a authority for 384
the international and interstate importation of live organisms (Schmitz and Simberloff 385
2001, Lodge et al. 2006), which ideally would also include intra-state movements of NIS. 386
387
Comparing invasions across multiple vectors – Apples and oranges 388
Although currently available data on NIS delivery by maritime vectors are too disparate 389
for a rigorous cross-vector risk assessment, this assessment provided some rough 390
comparisons across the vectors. Historical data indicate that ballast water, despite the 391
19
national and international focus on it as the primary vector for marine NIS, is by no 392
means necessarily the most important vector for established marine NIS in California 393
(figure 1). Indeed, this situation is likely true in other geographic locations (Bax et al. 394
2003). Managing ballast water, although necessary and an example of a vector-based 395
approach, is clearly insufficient to prevent new introductions given the importance of 396
other vectors. Although we found no common currency to allow highly quantitative 397
comparisons of contemporary NIS presence and abundances circulating in each vector 398
(figure 2), the available data support the conclusion that other vectors must be addressed 399
in addition to ballast water. Flux data support ornamental species as a potentially risky 400
vector (figure 2), which would not have been evident from historical data (figure 1). 401
402
Flux is often positively related to establishment rates (Colautti et al. 2006, Hayes and 403
Barry 2008, Simberloff 2009) and reducing or eliminating flux is a prime management 404
target. However, the risk of harm is also shaped in the consecutive stages along the 405
invasion pathway of entrainment, transport, and release into the environment, and the 406
contribution of each stage to overall risk differs among vectors (figure 5). Flux estimates 407
for ornamental, live bait, and live seafood species are not necessarily good predictors of 408
the probability that they will be introduced (released into the environment) because the 409
available data on flux reflect only part of the full journey from source to destination 410
waters (figure 5, #1, #2). Therefore, while these organisms are entering California, there 411
is no information on their release into marine and estuarine habitats until their 412
establishment as NIS is detected. Release rates are also unknown for marine ornamental 413
species; only a few rates exist for freshwater ornamentals (e.g., Strecker et al. 2011). 414
20
Despite the high flux of marine ornamental species and their hardiness, their 415
establishment has been low in California, perhaps because they are rarely released or that 416
most of the species are tropical and do not survive release or they are transferred out of 417
the state. 418
419
In contrast, ballast, fouling, and aquaculture organisms are released to, or directly 420
contact, marine environments. Vessel biofouling carries a large number of species and 421
individuals (high flux) but the quality of the vector’s habitat is variable for individuals, 422
some of which are undoubtedly lost en route (Murray et al. 2012). Aquaculture differs in 423
having a comparatively low flux but there is a strong economic incentive to ensure 424
survival. However, data are lacking on the numbers of permitted aquaculture organisms 425
that are actually placed in the environment (see above). 426
427
Marine NIS impacts in California 428
The ultimate goal of NIS risk assessment is to predict the probability of ecological, 429
economic, and social harm. The perception that harm will occur often drives responses to 430
invasions and motivates NIS management. Just as vectors differ in numbers and 431
frequencies of non-native species, the impact of non-native species might not be 432
delivered evenly among vectors. To assess whether the ecological and economic impacts 433
of marine NIS in California could be differentiated by vector, we completed BIOSIS 434
searches for impacts of mollusc, algal, and crustacean species (including alternate and 435
synonymous species names) from 1926 through 2011 (see Supplemental Material, Table 436
21
B for search protocol and references for results). These taxonomic groups represent the 437
majority of the NIS in California. 438
439
Published peer-reviewed information was too limited to assess the impacts of these taxa, 440
let alone by vector (Supplementary Material, Table B). The majority of the information 441
uncovered was devoted to only three or fewer species in each taxonomic group. Fifty 442
publications concerning impacts were available for 11 of the 41 established molluscan 443
species (Supplemental Material, Table B), with 34% of these publications devoted to one 444
species, Mytilus galloprovincialis. The impact literature on algal species produced similar 445
results, with three species (Caulerpa taxifolia, Sargassum muticum, Codium fragile 446
subspecies) dominating 84% of the 124 impact publications. Impact data were available 447
for just 17 out of 87 crustacean NIS, with 42% of papers dedicated to the European green 448
crab, Carcinus maenas. Because only 17 publications on molluscs, two on algae, and six 449
on crustaceans were specific to California, the relevance of the impact information may 450
be limited given impacts can be highly context-dependent (Thomsen et al. 2011). Without 451
better data, impacts cannot be apportioned across vectors, leaving vectors to be singled 452
out for their impacts one at a time. For example, the ornamental trade vector has stood 453
out as being responsible for introducing some of world’s worst aquatic invasive species 454
(Padilla and Williams 2004, Semmens et al. 2004), including the seaweed Caulerpa 455
taxifolia, which cost California over $6 million to eradicate (Anderson 2005) and lionfish 456
(figure 4). 457
458
459
22
Vector management led to temporal changes in flux- 460
To the extent they have been taken, management approaches have also varied by vector. 461
Although historically aquaculture and ballast water were potent vectors for marine NIS 462
introduction, these vectors have been deliberately interrupted to reduce their flux (figure 463
5, #3, #4). The drivers of change between historical and modern transport of bivalves and 464
ballast water differed considerably; aquaculture vector changes were driven by industry 465
practices and profitability, while the ballast water mechanism changed because of explicit 466
vector management policy and regulation. 467
468
Historically, aquaculture shipments were a stronger vector than today because the 469
intentional transfer of adult bivalve species was accompanied by an assortment of 470
unintentional “hitchhiking” species (figure 5, #3), which benefited from the high-quality 471
transport conditions needed for the bivalves. However, consciousness about NIS has 472
heightened in the aquaculture industry with the result that under current practices the 473
accidental introductions of associated species or ‘hitchhikers’, which were historically an 474
important source of NIS, are now minimal. The vast majority of contemporary bivalve 475
shipments consist of larvae or juveniles of one species, the commercial Pacific oyster 476
Crassostrea gigas, with few (if any) additional entrained species, resulting in a 477
dramatically lower risk of invasions (figure 5, #4). Analogous to current practices for 478
aquaculture shipments, the elimination of biological packing materials (seaweeds, Haska 479
et al. 2012) offers an opportunity to reduce the unintentional species that accompany 480
intentional bait shipments, which could slow transfers of NIS from New England and 481
Asia to California. 482
23
483
Historical ballast water entrained a large pool of planktonic species during a voyage that 484
was reduced in species richness and abundance upon discharge by the net effect of 485
interacting biological and environmental factors (figure 4, #5). The initiation of mid-486
ocean ballast water exchange (figure 4, #6) has reduced propagule delivery by enhancing 487
interruption of the transport phase. Today, international, federal, and state ballast water 488
regulations are among the few examples of active vector management in the marine 489
realm; however, establishing such management practices has been the result of an 490
arduous, ongoing, 30-year process. 491
492
A few marine and brackish ornamental species intended for sale or display are regulated 493
by California as restricted species (alligators, sharks, gars) and the state has enacted 494
legislation to ban importation, sale, and possession of nine species of the seaweed 495
Caulerpa (Assembly Bill 1334, chaptered in 2001, CDFG Code 2300). Neither 496
California’s nor the US Department of Agriculture’s Noxious Weed listing of Caulerpa 497
taxifolia (invasive Mediterranean strain, 1999) has been effective (Diaz et al. 2012). The 498
ornamental trade’s involvement in NIS management in California and elsewhere has not 499
been as strong as industry involvement has been for aquaculture and ballast water, which 500
is both a lesson to learn and an opportunity. 501
502
Conclusions 503
Way forward – Vector “blitz”, expert judgment, and management opportunities 504
24
Clearly, the many disparate sources of data available for each vector were not adequate 505
for a rigorous risk assessment of multiple vectors, even for just the initial steps of 506
entrainment and transfer of NIS in the invasion process, let alone their release and 507
impacts. To contend with the lack of a common currency for a cross-vector comparison 508
of the identity and abundances of organisms arriving in the multiple vectors and in 509
recognition that managers must prioritize resource allocation in data-poor situations, we 510
recommend a novel “vector blitz” to obtain comparable flux data rapidly and relatively 511
inexpensively. Rapid assessments or “BioBlitzes”, in which the number of newly 512
introduced and established NIS is quantified at a single field location over a short time 513
interval (days), are common (Delaney et al. 2008). In an analogous vector blitz, the 514
abundances and identity of organisms would be quantified in a coordinated manner 515
across vectors over a standardized time period and location using a standard sampling 516
unit to be resolved beyond the units we present in figure 3. While marine bioblitzes 517
characterize what NIS have already arrived, the vector blitz would characterize the names 518
and numbers of potential invaders on the way. Vector blitzes would force resolution of 519
the common currency problem. For example, should the number of vessels, their volume, 520
or wetted surface area be accounted for, or all three? The locale selected for the blitz 521
would need to be sufficiently large to encompass representative vectors. Shipping ports 522
generally do not support aquaculture because of poor water quality, but aquaculture often 523
occurs in nearby bays. For a Californian example, aquaculture in Agua Hedionda lagoon 524
and Tomales Bay is within striking distance of Los Angeles and San Francisco, 525
respectively. A rigorous vector blitz would provide a concrete measure of the cost 526
involved in collecting data for a longer-term cross-vector comparison or risk assessment. 527
25
Coordination of scientists, agency staff, and citizens would be necessary. Access to 528
commercial ports, marinas and small vessels would need to be secured, which was an 529
issue for our fishing vessel surveys. Taxonomic expertise would be required, as would 530
Institutional Review Board approval (for human subject research) to survey vendors of 531
seafood, bait, and ornamental species. A vector blitz is a perfect opportunity for a 532
targeted educational campaign to raise awareness of the multiplicity of vectors in 533
operation. Given a vector blitz would be the first of its kind, it would be a rigorous proof 534
of concept and a step toward defining a common currency for NIS fluxes. Thereafter, 535
however, vector blitzes should be repeated in time and space to capture the dynamics of 536
NIS introductions and vector operation to evaluate management efficacy and to 537
reprioritize vectors when necessary. 538
539
Although understanding the fluxes of organisms in vectors or propagule pressure is 540
critical to managing vectors, other differences among vectors influence the probability of 541
actual introduction, establishment, and impact. As we described earlier, these differences 542
are known only qualitatively. In this data-poor situation, the tool of expert judgment 543
offers a stopgap measure to help inform management decisions about vectors (Hayes 544
2002, Therriault and Herborg 2008, Acosta and Forrest 2009). Although expert judgment 545
is inherently subjective, prone to systematic errors, and can lead to false confidence in the 546
result, it can supplement limited data and help quantify uncertainties, as demonstrated in 547
recent applications of Bayesian models to invasive species (Kuhnert et al. 2010). Unlike 548
more commonly used statistical models, Bayesian models can incorporate prior 549
knowledge about the variables, such as the results of an expert judgment elicitation on 550
26
NIS release rates and impacts, into the model development. A cross-vector Bayesian risk 551
model for California’s maritime vectors is under development, based on our results and 552
expert elicitation. Limitations of expert judgment are being addressed (Burgman et al. 553
2011), but for now, expert judgment is a crutch and not a substitute for data-driven 554
management. 555
556
Despite major data gaps, there are clear examples of changes in vector operations that 557
have caused sustained vector disruption for both aquaculture and ballast water (figure 5) 558
and further management opportunities exist. Our analysis revealed that vessel biofouling 559
was and is a very strong vector, supporting a compelling need to reduce its NIS flux 560
associated with both commercial vessels and small crafts. Similar to the management 561
progress made for aquaculture and ballast water, managing vessel biofouling to induce 562
more regular maintenance of submerged surfaces of commercial vessels and transient 563
boats could reduce propagule delivery (Johnson and Fernandez 2011). A number of 564
countries have recognized that managing the biofouling on ships' hulls can reduce the risk 565
of marine invasions (Gollasch 2002, Floerl et al. 2005, Hewitt et al. 2009). In 2011, the 566
International Maritime Organization adopted biofouling management guidelines for ships 567
>24 m, which are primarily commercial vessels, and is working on guidelines for smaller 568
vessels. California now requires periodic removal of hull fouling organisms for vessels 569
over 300 gross registered tons and capable of carrying ballast water. An annual hull 570
husbandry report would also be required to enable better understanding of the extent of 571
the hull fouling flux in California (3 July 2013; 572
http://www.slc.ca.gov/spec_pub/mfd/ballast_water/Documents/FoulingInfoSheet.pdf). 573
27
574
Our multi-vector analysis also revealed that reducing the risk from biofouling requires 575
managing not only large vessels but also small craft. The small craft vector has roughly 576
the same magnitude of vessels traveling from out-of-state as the commercial vessel vector 577
(table 1, figure 2). These vessels can accumulate high biofouling loads when they sit in 578
harbors for long periods (figure 6), yet they have not received any substantial 579
management attention or even sustained outreach on NIS transfers to promote cleaner 580
submerged surfaces, with the exception of efforts by the cooperative extension unit in 581
California’s Sea Grant Program [3 July 2013; http://ca-sgep.ucsd.edu/focus-582
areas/healthy-coastal-marine-ecosystems/healthy-ecosystems-boating]. Our analysis 583
highlights the need for better data on the movements of small crafts and the extent of 584
biofouling to determine whether prioritization of this sector of the vector is merited. 585
586 Given that the majority of established species are associated with multiple vectors, the 587
key to reducing future rates of new NIS introductions is to move away from approaches 588
that target only commercial shipping and toward a more diversified approach that tackles 589
all vectors simultaneously, or if sequentially, then in a prioritized manner, for example 590
addressing biofouling of all vessel types next. Efficient, effective management is difficult 591
to envision in the absence of good data and also an authority with the resources and 592
accountability for the management of the multiple vectors in operation. Vector blitzes 593
would result in better, more comparable data for estimating the flux of NIS arriving in 594
multiple vectors, as required for a quantitative cross-vector risk assessment. Centralized 595
permitting and data collection for NIS-associated sales of live bait, seafood, aquaculture, 596
and ornamental species could also yield more standardized data. The need for centralized 597
28
regulatory authority is highlighted in the aquaculture example (figure 3), to echo 598
recommendations repeatedly put forth (Schmitz and Simberloff 2001, Lodge et al. 2006). 599
Severe impediments to centralization are the expense and effort to reorganize government 600
bureaucracies and to fund external contractors, which has contributed to the expiration of 601
several useful NIS web sites. In California, the Ocean Protection Council is serving at 602
least in a centralized advisory role for maritime NIS. A more flexible and perhaps less 603
costly alternative to centralization is a network of information distributed from nodes 604
representing sites where data are collected routinely across vectors (Ruiz and Carlton 605
2003), ideally in standardized vector blitzes. Each node could be funded independently 606
and the loss of one would be a regrettable data gap but would not collapse the entire 607
network. 608
609
Maritime NIS risk assessment has been moving from single-species approaches to 610
considering entire vectors (Floerl et al. 2009, Chan et al. 2012). The next opportunity for 611
advancement in theory and practice lies in developing a rigorous assessment of multiple 612
species in multiple vectors that represent the cumulative risk NIS pose in California and 613
elsewhere. There is no substitute for good data, and our analysis highlights the need to 614
establish a common currency to compare NIS abundances in different vectors and to 615
collect data on NIS release rates. The invasion process is understood very well and there 616
are good models and frameworks for how vector management can work, conceptually 617
and practically. We need to join the various disparate components into an integrated 618
system, allowing a strong basis for prioritization and science-based decisions for vector 619
29
management --- leaving behind the current ad hoc approach that leaves the door open to 620
new invasions. 621
622
Acknowledgments 623
This work was supported by Proposition 84 funds made available to the California Ocean 624
Science Trust by the California Ocean Protection Council with additional funding from 625
the California Ocean Science Trust, the California Sea Grant Program, and the 626
Smithsonian Institution. We thank many staff in federal and state agencies for their 627
generous assistance, especially G. Townsend and K. Ramsey. Ocean Science Trust staff 628
facilitated and helped shape the work, in particular S. McAfee, R. Gentry, E. Kramer-629
Wilt, and R. Meyer. We thank P. Fofonoff, K. Holzer, and B. Steves for critical database 630
support. We also thank anonymous reviewers and T. Beardsley for clarifying comments. 631
632
Supplemental Materials 633
Table A. Non-indigenous estuarine and marine invertebrates and algal species established 634
in California. 635
Table B. Literature search methodology and resulting references for information on 636
impacts of marine and estuarine NIS molluscs, crustaceans, and algae 637
established in California. 638
639
30
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819
38
Table 1. Comparison of vessel data used in Figure 2. This table provides details of the 820
parameters and sources for vessel vectors that provide some of the basis for Figure 2. It 821
also highlights the disparate nature of vector data, even among a subset of similar vectors. 822
823
Recreational Fishing Commercial
# vessels 1182 134 1822
# arrivals in CA Unknown Unknown 6002
Origin Foreign OR, WA Outside CA
Date 2009 2008 2010
Data source CBP PacFIN NBIC
Fouling organism abundance
Abundance per vessel
sampled
# vessels # vessels # vessels
0 7 unknown 2
1-10 11 unknown 2
11-100 6 unknown 0
101-1000 13 unknown 2
1001-10,000 7 unknown 8
10,001-100,000 3 unknown 7
> 100,000 2 unknown 2
Total vessels sampled 49 0 23
% with fouling NIS 86 unknown 68
39
Arrivals discharging
non-CA sourced water Not applicable Not applicable 962
% with ballast NIS Not applicable Not applicable Unknown
824
‘CBP’, Customs and Border Protection; ‘PacFin’, Pacific Fisheries Information 825
Network; ‘NBIC’, National Ballast Information Clearinghouse; ‘NIS’, non-826
indigenous species. 827
Note: No data were available for arrivals of fishing vessels from regions other than 828
Oregon and Washington, although arrivals probably occur. 829
830
40
Figure 1. Vector attributions by taxa. (a) 90 marine NIS species established (including 831
two subsequently eradicated) in California were attributed solely to a single vector 832
(“single-vector species”). The “Protozoans” include Ciliophora. (b) 145 NIS in California 833
were associated with two or more vectors (“multiple-vector species”). The graphed total 834
exceeds 145 species because each species was assigned to all of the vectors considered 835
possible transfer mechanisms at each location (n = 389 events). (c) For multiple-vector 836
species (as in panel b), vector attribution was apportioned to each species by the number 837
of unique place-times each vector was associated with an introduction. Taxa with < 10 838
species: “other”. “Unascribed”: a vector was not assigned to a species in the NEMESIS 839
database (Supplemental material, Table A). 840
841
Figure 2. Annual NIS flux across vectors. Data illustrating the lack of a standardized 842
metric to compare propagule flux across vectors: biofouling (recreational, fishing, and 843
commercial vessels), ornamental species trade, aquaculture, and ballast water discharge 844
as: (a) arrivals of units that could be managed for each vector (where available for 845
biofouling, both the number of unique vessels (solid) and estimated number of arrivals 846
(diagonal) are shown), (b) propagule flux associated with each arrival unit in panel a 847
(kite diagrams illustrate the distribution of frequencies), and (c) likelihood of NIS 848
associated with each unit of introduction. Note log scales in panels (a) and (b). Date 849
range or the number of vessels sampled is indicated at the top of the figures. Fill indicates 850
certainty, for example, we are confident of the number of ships discharging ballast into 851
California waters (black), but accurate information concerning aquaculture permits in the 852
state was not available (gray). White fill indicates ballast water data are from non-853
41
California ports. No data were available for the number of individuals delivered by 854
aquaculture or fishing vessels or the proportion of NIS in ballast water or fishing vessel 855
fouling communities. See Table 1 for vessel data summary. 856
857
Figure 3. The process for importing animals and marine plants into (or moving within) 858
California for aquaculture purposes. Dashed lines indicate import regulations for plants. 859
Plants and animals imported into the United States must be cleared by the USFWS and/or 860
the USDA. The California Department of Food and Agriculture (CDFA) maintains a 861
noxious weeds list of species prohibited for importation. There are no restrictions on 862
moving aquaculture species within the state. Marine animals and plants intended for 863
placement into state waters must also be permitted through CDFG (Import Permit) if 864
moved from out of state. CDFG Private Stocking Permits are required for organisms used 865
for non-commercial purposes. Commercial facilities must file a management plan with 866
the California Department of Health. CDFG manages aquaculture leases; leasees must 867
file an annual Proof of Use Report. The ACE requires permits for structures placed in the 868
water. Despite the numerous permits required in some cases, complete data on the source, 869
species, and numbers of individuals actually placed in the water are not collected. 870
871
Figure 4. Lionfish (Pterois volitans) in its native Indo-Pacific region. Lionfish are an 872
ornamental species that invaded the Caribbean, Gulf of Mexico, and US eastern seaboard. 873
They can tolerate temperate waters and are being imported into California. Photographer: 874
Bruce Nyden. 875
876
42
Figure 5. Conceptual diagram comparing maritime vectors and potential management 877
control points. Eight contemporary maritime vectors (left column) are compared across 878
(a) the relative size of source propagule pools (left-hand circles), (b) typical transit 879
processes (polygons in middle section), and (c) relative inocula sizes during propagule 880
delivery (right-hand circles). White circles and polygons: target species pools and 881
deliberate transfer activities during intentional vector processes; gray circles and 882
polygons: unintentional transfers of species; hatched polygons: intentional transfers of 883
species with associated unintentional transfers. Circle diameter (left side) represents 884
estimated species richness at the beginning of a typical transfer (small, medium, large 885
circles reflect 1 – 9, 10-99, and 100-1000 species per shipment). For example, shipping 886
vectors (ballast water and biofouling) and shipments of ornamental species are 887
considered at present to have the highest richness while contemporary bivalve 888
aquaculture shipments are single species transfers. Contemporary shipments of live bait 889
include the target bait species and the associated unintentional entrainment of non-target 890
species in packing material (1). A large influx of species via the seafood, ornamental, and 891
bait vectors arrive into terrestrial hubs (airports, wholesalers) followed by an unknown 892
attrition rate with releases into the sea by end-users (2). Biofouling of commercial, 893
recreational, and fishing vessels transfers species into and within the state with invasion 894
opportunities enhanced by constant vector contact with the marine environment. The 895
dashed-line box shows historical operation of aquaculture (3) compared to the present (4) 896
and historical ballast water (5) operation compared to modern (6). 897
898
43
Figure 6. Heavy biofouling on the hull of a transient recreational boat in California. 899
Photographer: Ian Davidson. 900
901
44
902
Figure 1. 903
0 20 40 60 80 100
a
0 20 40 60 80 100
b
0 20 40 60 80 100
c
Seafood
Ornamental
Bait
Unascribed
Aquaculture
Ballast
Biofouling
Other
single-vector species
number of species
Crustaceans
Ectoprocts
Tunicates
Molluscs
Platyhelminthes
Protozoans
Other
Cnidarians
Annelids
Algae
Seafood
Ornamental
Bait
Unascribed
Aquaculture
Ballast
Biofouling
Other
number of species
number of weighted species
many-vector species
many-vector species
Seafood
Ornamental
Bait
Unascribed
Aquaculture
Ballast
Biofouling
Other
45
904
905
Figure 2. 906
907
Recreational
Annu
al sh
ipmen
ts
1
10
100
1,000
10,000
ORNAMENTAL AQUACULTURE BALLASTFishing Commercial
Annu
al im
port permits
Annu
al sh
ips d
ischarging
Annu
al vessels arriving
10-‐100
103-‐104
Individu
als p
er arrival
Individu
als p
er sh
ipmen
t
Individu
als p
er permit
Individu
als p
er discharge
100
% with
NIS
0
20
40
60
80
0
20
40
60
80
% with
NIS
BIOFOULING
Unknown
1
10
100
1,000
10,000
1
10
100
1,000
10,000
1
10
100
1,000
10,000
0
20
40
60
80
% with
NIS
% with
NIS
Unknown
a
b
c
105-‐106
107-‐108
0 0
105-‐106
107-‐108
10-‐100
0
107-‐108
Unknown
10-‐100
103-‐104 103-‐104
2009 2008 2010 2009 2009 2010
n=49 n=23 2009 <2005
n=49 n=23 2009 2009
Unknown
Recreational
Annu
al sh
ipmen
ts
1
10
100
1,000
10,000
ORNAMENTAL AQUACULTURE BALLASTFishing Commercial
Annu
al im
port permits
Annu
al sh
ips d
ischarging
Annu
al vessels arriving
10-‐100
103-‐104
Individu
als p
er arrival
Individu
als p
er sh
ipmen
t
Individu
als p
er permit
Individu
als p
er discharge
100
% with
NIS
0
20
40
60
80
0
20
40
60
80
0
20
40
60
80
% with
NIS
BIOFOULING
Unknown
1
10
100
1,000
10,000
1
10
100
1,000
10,000
1
10
100
1,000
10,000
1
10
100
1,000
10,000
1
10
100
1,000
10,000
1
10
100
1,000
10,000
0
20
40
60
80
0
20
40
60
80
% with
NIS
% with
NIS
Unknown
a
b
c
105-‐106
107-‐108
0 0
105-‐106
107-‐108
10-‐100
0
107-‐108
Unknown
10-‐100
103-‐104 103-‐104
2009 2008 2010 2009 2009 2010
n=49 n=23 2009 <2005
n=49 n=23 2009 2009
Unknown
46
908
Figure 3. 909
910
CDFG: Import Permit(annual permit)
Non-commercial useCDFG:
Registeredaquaculture
facility
CDFG managed lease
CA Department of Health(management plan)
Other than CDFGmanaged lease
CDFG:Private Stocking Permit
CDFG: Proof of Use Report (annual report)
Structures in water No structures in water(no permit required)
US Army Corps of Engineers(5 year permit)
Animal
From overseas From outside of California Within California(no regula!ons)
Marine plant
USFWS clearanceUSDA/USFWS clearance
(Federal Noxious Weed Act)or CDFA (state list) clearance
CDFA (state list) clearance
47
911 912
Figure 4. 913
914
48
915 916 Figure 5. 917
49
918 919 Figure 6. 920 921
