781 A qualitative biological risk assessment for vase tunicate Ciona intestinalis in Canadian waters: using expert knowledge Thomas W. Therriault and Leif-Matthias Herborg Therriault, T. W., and Herborg, L-M. 2008. A qualitative biological risk assessment for vase tunicate Ciona intestinalis in Canadian waters: using expert knowledge. – ICES Journal of Marine Science, 65: 781 – 787. Keywords: Ciona intestinalis, ecological risk, genetic risk, invasive species, risk assessment, vase tunicate. Received 18 June 2007; accepted 25 February 2008; advance access publication 17 April 2008. T. W. Therriault and L-M. Herborg: Pacific Biological Station, 3190 Hammond Bay Road, Nanaimo, BC, Canada V9T 6N7. Correspondence to T. W. Therriault: tel: þ1 250 7567394; fax: þ1 250 7567138; e-mail: thomas.therriault@dfo-mpo.gc.ca. Introduction Non-indigenous species (NIS) can pose an enormous risk to the integrity of native ecosystems (Sala et al., 2000), and global invasions appear to be accelerating (Ruiz et al., 2000). However, not all introductions pose the same level of risk, because some NIS fail to establish or to attain population proportions that lead to ecological or economic impacts (Williamson, 1996). Therefore, it is important to characterize the potential risk posed by a NIS in a timely manner, especially if management or mitigation measures are to be undertaken. Typically, this is done using a risk assessment, whereby both the probabilities (likelihoods) and consequences (impacts) of an invasion are characterized. By considering the general phases of an invasion event, there is a hierarchy within which risk can be considered formally (Lockwood et al., 2005; Holt, 2006). Generally, NIS risk assessments characterize the potential for arrival, survival, reproduction, and spread (filters in the invasion process), and the potential impacts (ecological, genetic) associated with an introduction (Hayes, 1998; Lockwood et al., 2005). The risk assessment presented here is adapted from the process outlined in the two-part Canadian National Code on Introductions and Transfers of Aquatic Organisms, which was designed for intentional releases (DFO, 2003), so characterizing the probability of arrival was a necessary addition for unintentional introductions. Part I of the Code evaluates the probability and consequence of the establishment of an aquatic organism, and Part II evaluates the probability and consequence of the establishment of a pathogen, parasite, or fellow traveller of the aquatic organism. In each part, # 2008 two component ratings are determined and combined to determine the overall level of risk: high (organism of major concern, management/intervention required), moderate (organism of intermediate concern, management/intervention probable), or low (organism of little concern, management/intervention unlikely). Additionally, an uncertainty level is assigned ranging from very low (i.e. certain with a scientific basis) to very high (i.e. highly uncertain or “best guess”). Ciona intestinalis has been identified on both sides of the North Atlantic, in North America and Europe (Millar, 1966; NIMPIS, 2002), but extensive debate has not resolved the native range of this species. Consistent with others, we classify it as a cryptogenic species (NIMPIS, 2002) until its native range can be resolved. It has spread to the west coast of North America, South America, Australia, New Zealand, Asia, and Africa (Kott, 1990; NIMPIS, 2002; Lambert and Lambert, 2003), primarily as a fouling species on commercial vessels or associated with aquaculture transfers (Cohen et al., 2000). In its invaded range, C. intestinalis has had negative ecological consequences, including impacts on shellfish aquaculture (Uribe and Etchepare, 2002; Carver et al., 2003; Ramsay et al., in press), as well as on native species diversity and ecosystem processes (Blum et al., 2007). Ciona intestinalis has broad environmental tolerances, especially temperature and salinity (Dybern, 1965; Carver et al., 2003), which partially explains its cosmopolitan distribution. Applying different environmental models, Therriault and Herborg (2008) identified many potentially suitable habitats along both Atlantic and Pacific coasts of Canada. Ciona savignyi, a congener that is frequently confused International Council for the Exploration of the Sea. Published by Oxford Journals. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org Downloaded from https://academic.oup.com/icesjms/article/65/5/781/714476 by guest on 25 March 2024 Non-indigenous species (NIS) can pose a significant level of risk, through potential ecological or genetic consequences, to environments to which they are introduced. One way to characterize the overall risk posed by a NIS is to combine the probability and consequences of its establishment in a risk assessment that can be used to inform managers and policy-makers. The vase tunicate Ciona intestinalis is considered to be a cryptogenic species in eastern Canadian waters, but has not yet been reported from Pacific Canada. Because it is unclear what level of risk it poses for Canadian waters, we conducted a biological risk assessment for C. intestinalis and its potential pathogens, parasites, and fellow travellers. An expert survey was conducted to inform the risk assessment. The ecological risk posed by C. intestinalis was considered high (moderate uncertainty) on the Atlantic coast, and moderate (high uncertainty) on the Pacific coast. The genetic risk posed by C. intestinalis was considered moderate on both coasts, with low uncertainty on the Atlantic coast and high uncertainty on the Pacific coast, where hybridization with Ciona savignyi may be possible. Pathogens, parasites, and fellow travellers were considered to be a moderate ecological risk and a low genetic risk (with high uncertainty) for both coasts. 782 Material and methods Expert survey Given the recent invasion history of C. intestinalis, much of the information required to inform the risk assessment process might remain unknown, based on a search of traditional literature reviews. Therefore, we supplemented the information collected from the literature with an online survey of experts. Our target experts were familiar with invasive tunicates, aquatic invasive species, or risk assessment. Our online questionnaire was designed in Survey Monkey (www.surveymonkey.com), and the web link was sent to 520 experts and three mailing lists (ALIENS-L, Tunicata, and CAISN) associated with either tunicates or invasive species. Each respondent was asked to identify their level of expertise as either species-specific for any of five tunicates considered (C. intestinalis, Styela clava, Botryllus schlosseri, Botrylloides violaceus, and Didemnum sp.); group-specific (colonial vs. solitary tunicates), or tunicates in general. This design meant that each expert answered questions appropriate to their level of knowledge. Each was then asked to provide responses on potential vectors and impacts at their level of knowledge. Ten potential vectors for dispersal were considered: larval drift, dispersal of adults attached to flotsam, ballast water, movement of aquaculture gear and stock, fragments in fishing gear, aquarium releases, intentional release to establish a food source, hull fouling on slow-moving barges, and hull fouling of large (.50 m) and small (,50 m) vessels. Respondents were asked to provide an estimate of the importance of each vector and the uncertainty associated with their reply. They were provided with definitions for vector importance and uncertainty (Appendix), and they had a choice of five answers: very high, high, medium, low, and very low. Further, respondents were asked to state, in their opinion, what impact invasive tunicates could have on biodiversity, marine protected areas, shellfish aquaculture, finfish aquaculture, commercial fisheries, vessels/moorings, and recreational activities (boating, fishing, diving, etc.). As with vector importance, we wanted to measure the potential uncertainty of these impacts, so respondents also were asked to identify the likelihood of these impacts (Appendix). Categorical responses were converted to numerical values and averaged to determine the mean respondent value for each variable in our survey. Figure 1. Heat matrix used to combine the probability of introduction and the ecological or genetic consequences of introduction to determine an overall level of risk posed by Ciona intestinalis in Canadian waters. Overall risk is high (dark grey), moderate (grey), or low (light grey). Risk assessment Risk has two components: probability and impact. The overall level of risk posed by a NIS is a combination of the probability of establishment and the consequences of that establishment. We combined these two categorical scores using a heat matrix (Figure 1), which allows the evaluation of the relative contributions of each component score to the overall score qualitatively. Overall risk increases from the lower right to the upper left of the matrix, where 50% of the cells represent moderate risk and the remaining cells represent high (25%) or low (25%) risk. Within the probability of establishment, four major components represent filters in the invasion process. All are determined in terms of probability or likelihood that the NIS will: (i) arrive in the geographical area being considered by the risk assessment; (ii) survive where it is introduced; (iii) reproduce within the introduced environment in order to establish a population; (iv) spread from the initial introduction location. The second component of the overall level of risk is the consequences of a NIS establishing. Specifically, what are the ecological or genetic consequences on native ecosystems or stocks if a NIS is able to establish? Results Expert survey We received 132 replies to our survey, of which 41% had speciesspecific knowledge, 16% had group-specific knowledge (colonial vs. solitary tunicates), and 42% had general tunicate knowledge. The respondents identified their main expertise as marine organisms (87%), ecology (68%), invasive species (68%), and risk assessment (20%), noting that multiple answers were possible. Of the respondents, 21 had species-specific knowledge for C. intestinalis, 14 had group-specific knowledge for solitary tunicates, and 27 had general tunicate knowledge. The survey identified several vectors that are potentially important for the introduction or, in most cases, secondary spread of C. intestinalis. Hull fouling on slow-moving vessels (e.g. barges) was considered the most important vector by all experts, regardless of their expertise. Also, aquaculture-related transfers, followed by hull fouling on small Downloaded from https://academic.oup.com/icesjms/article/65/5/781/714476 by guest on 25 March 2024 with C. intestinalis, is a non-indigenous tunicate from Asia that is widely distributed along the Pacific coast from Alaska to southern California (Lamb and Hanby, 2006), suggesting that additional suitable habitat may exist for C. intestinalis, if tolerances are similar. Here, we present a biological risk assessment for C. intestinalis in Canadian waters. We identify the overall risk potential for the species and its associated pathogens, parasites, and fellow travellers, and we identify uncertainty for each step in the risk assessment. Further, the goal of this risk assessment was to identify and characterize the biological risk it poses in Canada. Socio-economic factors are important in an overall risk analysis framework, but are beyond the scope of the biological risk assessment presented here. As C. intestinalis has recently impacted shellfish aquaculture operations in Atlantic Canada (Carver et al., 2003) and has not been reported from Pacific Canada, a biological risk assessment can inform managers and policy-makers on the potential risk that the species poses to Canadian waters. T. W. Therriault and L-M. Herborg 783 Qualitative biological risk assessment for Ciona intestinalis in Canada Risk assessment Probability and consequences of C. intestinalis establishment Given that C. intestinalis has been reported on the Atlantic coast of Canada, it is certain that the species can survive and reproduce there (Millar, 1966). Given the presence of populations on the Atlantic coast (both Canadian and USA) combined with potential vectors, including slow-moving commercial and recreational watercraft and various aquaculture activities, and areas of good environmental suitability (Therriault and Herborg, 2008), there is a great probability that C. intestinalis will spread along the Atlantic coast. This would include the spread to additional areas where the species may not have been reported yet, such as bays around Prince Edward Island (Ramsay et al., in press). Areas of environmental suitability also exist in Pacific coastal waters (Therriault and Herborg, 2008), and an abundance of potential vectors exist within this region that could be used by C. intestinalis to establish populations or to spread along the west coast, namely recreational watercraft, the transfer of aquaculture product or gear, and tug and barge activity, each of which was ranked high in our survey (Table 1). The probability of the arrival of C. intestinalis to Canadian west coast waters was considered high because of the presence of established populations along the west coast of the USA, including populations reported near the Canadian border in Puget Sound, WA (G. Lambert, pers. comm.), and farther south in California (Lambert and Lambert, 2003), and the existence of suitable vectors. Intracoastal commercial and recreational shipping between USA and Canadian waters along the west coast is a likely pathway for introduction (Verling et al., 2005), especially commercial barge traffic between Puget Sound and the Strait of Georgia (Port of Vancouver), owing to the short transit time and slow speeds that are unlikely to dislodge many “hitch-hikers”. Moreover, arrival from either its cryptogenic or invaded range outside North America should not be dismissed. Overall, the probability of establishment of C. intestinalis is very high for the Canadian Atlantic coast (already present) and high for the Canadian Pacific coast (Table 3). The most severe impacts of C. intestinalis worldwide have been on shellfish aquaculture production (Uribe and Etchepare, 2002; Carver et al., 2003; Ramsay et al., in press), but as a highly competitive species within subtidal, epibenthic communities, it has displaced native species, lowered biodiversity, and altered community properties in some invaded habitats (Blum et al., 2007). Aquaculture impacts and impacts on native biodiversity also ranked moderate to high in our expert survey (Table 2). Other ecological consequences include general competition for food and space, which can have cascading ecological impacts (Osman et al., 1989; Bingham and Walters, 1989). In addition to competition with native species, there also could be competition with other non-native species (e.g. C. savignyi or S. clava). For example, studying a C. intestinalis population in Denmark, Petersen and Riisgård (1992) estimated a maximum filtration potential equivalent to the volume of the cove per day, suggesting that grazing impacts on phytoplankton could be substantial. Therefore, the ecological consequences posed by C. intestinalis would be moderate (Table 3); impacts would be measurable and widespread (Appendix). There are no species similar to C. intestinalis in Atlantic Canada, so its potential for causing genetic consequences in Atlantic Canadian waters is very low (Table 3). However, on the Table 1. Responses to the expert survey on the importance of a range of potential vectors for the spread of invasive tunicates. Potential vectors Responses for Ciona intestinalis (n 5 20) Responses for solitary tunicates (n 5 14) Responses for general tunicates (n 5 27) Vector Vector Vector Vector Vector Vector importance uncertainty importance uncertainty importance uncertainty Natural larvae dispersal 3.00 3.67 3.38 3.62 3.24 3.15 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . Natural adult dispersal by drift 2.79 3.33 3.18 3.27 3.68 2.77 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . Ballast water release 2.47 2.56 2.92 3.17 3.36 3.00 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . Hull fouling of large vessels (.50 m) 2.94 3.28 3.82 3.55 3.85 3.11 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . Hull fouling of small vessels (,50 m) 3.42 3.53 3.82 3.27 3.73 2.85 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . Hull fouling of slow-moving vessels 4.20 3.70 4.18 3.73 3.96 2.81 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . Aquaculture transfers 4.00 3.53 4.17 3.75 3.78 2.81 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . Commercial fishing 3.37 2.94 2.90 3.30 2.81 2.52 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . Aquarium releases 1.59 2.13 1.82 3.00 1.92 2.46 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . Intentional releases to establish a food source 1.25 2.50 1.50 3.25 1.92 2.23 Respondents had the choice of answering species-specific questions for Ciona intestinalis, for solitary tunicates, or for tunicates in general. The three vectors with the greatest importance for tunicate dispersal, and the three replies with the least uncertainty are emboldened. Responses for vector importance were ranked as: very low ¼ 1, low ¼ 2, medium ¼ 3, high ¼ 4, very high ¼ 5. The uncertainty associated with the response was ranked as: very high ¼ 1, high ¼ 2, medium ¼ 3, low ¼ 4, very low ¼ 5 (detailed definitions are provided in the Appendix). Downloaded from https://academic.oup.com/icesjms/article/65/5/781/714476 by guest on 25 March 2024 vessels and/or large vessels, were identified as having a high potential to introduce or spread C. intestinalis in Canadian waters (Table 1). In contrast, aquaria and intentional release were identified as having the lowest potential to introduce or spread C. intestinalis (Table 1). The respondents to species- and group-specific questions felt most confident (i.e. least uncertain) in their estimates of vector importance for hull fouling of slow-moving vessels and aquaculture transfers. Experts who replied to general tunicate questions had the greatest confidence in their responses about hull fouling of large vessels and ballast water releases. In addition to the potential vectors for C. intestinalis spread, the survey collected information on several potential impacts of C. intestinalis introductions. High impact on shellfish aquaculture was reported by all groups of experts. Moderate-to-high impacts were noted for biodiversity, vessels and moorings, and finfish aquaculture (Table 2). The lowest impact uncertainty was in almost all cases associated with the highest impacted category (Table 2). 784 T. W. Therriault and L-M. Herborg Table 2. Responses to the expert survey on the potential magnitude of the impact of invasive tunicates. Potential impact Responses for Ciona intestinalis (n 5 21) Responses for solitary tunicates (n 5 13) Responses for general tunicates (n 5 25) Impact level Impact uncertainty Impact level Impact uncertainty Impact level Impact uncertainty Biodiversity 2.95 2.79 2.73 2.91 3.14 3.00 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Marine protected areas 2.56 2.27 2.40 2.60 2.91 2.73 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Shellfish aquaculture 4.00 3.45 4.46 4.15 4.04 3.64 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Finfish aquaculture 2.93 2.60 2.75 3.17 2.67 2.81 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Commercial fishing 1.93 2.00 1.83 2.33 2.47 2.58 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Vessels/Moorings 2.94 2.89 3.00 3.75 2.96 3.35 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Recreational activities 1.89 2.17 2.18 2.73 2.10 3.10 Table 3. Summary of risk scores used to determine the overall risk potential for Ciona intestinalis and pathogens, parasites, or fellow travellers associated with it. Element Atlantic coast Risk score Pacific coast Uncertainty Risk score Uncertainty Ciona intestinalis Arrival Very high Very low High High . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . Survival Very high Very low High Moderate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . Reproduction Very high Very low High Moderate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . Spread Very high Very low Moderate High . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . Overall estimate Very high Very low High High . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . Ecological Moderate Moderate Moderate Moderate consequence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . Very Low Low Low Low Genetic consequence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . Pathogen, parasite, or fellow traveller ............................................................................................................................... Arrival Low High Low High . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . Survival Low High Low High . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . Reproduction Low High Low High . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . Spread Low High Low High . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . Overall estimate Low High Low High . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . Moderate High Moderate High Ecological consequence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . Low High Low High Genetic consequence ............................................................................................................................... Arrival, survival, reproduction, and spread are combined to determine the overall estimate for the probability of establishment. Canadian Pacific coast there is another member of the family Cionidae, C. savignyi, also non-indigenous to Pacific Canadian waters. The two species are morphologically similar, resulting in considerable taxonomic uncertainty and frequent misidentification. Although hybridization has been reported for some marine taxa, notably Mytilus (McDonald et al., 1991), hybridization appears to be rare among tunicate species and has been reported not to take place between C. intestinalis and C. savignyi (Byrd and Lambert, 2000). Therefore, the potential genetic consequences of a C. intestinalis introduction to the Canadian Pacific coast should be considered low (Table 3). Probability and consequences of the establishment of pathogens, parasites, and fellow travellers of C. intestinalis Little is known about the parasites and pathogens of C. intestinalis. As yet, no diseases have been documented in C. intestinalis, but the species is known to possess parasitic or commensal copepods belonging to the order Doropygidae (Millar, 1971). Several copepod species have been identified as being associated with the branchial sac, including Pachypygus gibber, Hermannella rostrata, and Lichomolgus canui (Becheikh et al., 1996; Pastore, 2001), and Ooishi and O’Reilly (2004) isolated Haplostoma eruca from the intestine. Tan et al. (2002) reported that fouling of nets by C. intestinalis increased the risk of disease to farmed salmon in Tasmania, because C. intestinalis serves as a repository for the amoeba that is responsible for amoebic gill disease (AGD). For solitary tunicates transported as fouling organisms, it is usually their progeny that become established in new locations, rather than dislodgement of the individual itself. This dramatically reduces the probability that a pathogen, parasite, or fellow traveller will be introduced at the same time, because larval stages of marine invertebrates are often assumed to be relatively unsusceptible to these agents. Based on limited information, it is unknown how species-specific the commensal copepods of C. intestinalis are, or if they would encounter other susceptible organisms. For example, if the size of the branchial sac is limiting for these commensal copepods, are there ascidians present that attain a size similar to C. intestinalis, such that potential suitable hosts exist? In addition to some native ascidians, S. clava, another nonindigenous tunicate on both Atlantic and Pacific coasts, and C. savignyi, a non-indigenous tunicate on the Pacific coast, could represent potentially suitable hosts for these commensal copepods. Similarly, it is possible, albeit unlikely, that the amoeba responsible for AGD could be transported with C. intestinalis to finfish aquaculture sites in Atlantic or Pacific Canada. Therefore, the probability that a pathogen, parasite, or fellow traveller will be introduced is low, but uncertainty is high because available information is limited (Table 3). It is probable that the commensal species could be rather host-specific and that ecological or genetic impact on native species and ecosystems would be minimal. However, given the presence of extensive finfish aquaculture at some locations, infestation of C. intestinalis harbouring this amoeba could negatively impact salmon aquaculture. Therefore, the ecological consequences of Downloaded from https://academic.oup.com/icesjms/article/65/5/781/714476 by guest on 25 March 2024 Respondents had the choice of answering species-specific questions for Ciona intestinalis, for solitary tunicates, or for tunicates in general. The three areas with the greatest potential impact and the three areas with the least uncertainty are emboldened. Responses for impact level were ranked as: positive impact ¼ 0, very low negative ¼ 1, low negative ¼ 2, moderate negative ¼ 3, high negative ¼ 4, very high negative ¼ 5. The uncertainty associated with the response was ranked as: unlikely ¼ 1, possible ¼ 2, likely ¼ 3, almost certain ¼ 4, certain ¼ 5 (detailed definitions are provided in the Appendix). Qualitative biological risk assessment for Ciona intestinalis in Canada pathogens, parasites, and fellow travellers associated with C. intestinalis are moderate, but because of the paucity of available data, the uncertainty associated with potential consequences is high (Table 3, Appendix). It is unclear how either the commensal copepods or the pathogenic amoeba would negatively impact the genetic structure of native copepod or amoeba populations. Hence, the genetic consequences of these organisms is considered low, but again because of the paucity of available data, uncertainty is high (Table 3, Appendix). Overall level of risk Overall risk was determined using the heat matrix for both Atlantic and Pacific Canadian waters, including the risk posed by C. intestinalis and its potential pathogens, parasites, and fellow travellers, using the categorical responses summarized in Table 3. Overall ecological risks posed by C. intestinalis were high for the Atlantic coast and moderate for the Pacific coast, whereas genetic risks were moderate for both coasts (Figure 2). The risks posed by pathogens, parasites, and fellow travellers of C. intestinalis were the same for both coasts: moderate for ecological, low for genetic (Figure 2). Discussion The overall level of risk posed by the establishment of C. intestinalis in Canadian waters was moderate for the Pacific coast and high for the Atlantic coast. Therefore, this species should be considered as a major concern for Atlantic Canada, where intervention to mitigate the potential consequences will be required. In fact, the species has already plagued shellfish aquaculture operations in Atlantic Canada by outcompeting cultured mussels, and mitigation strategies are being explored (Carver et al., 2003). The difference in overall risk scores between coasts was expected, given that C. intestinalis has established populations in Atlantic Canadian waters and is spreading, based on recent accounts (Locke et al., 2007), but has yet to invade Pacific Canadian waters. Therefore, efforts should be directed towards lowering the probability of arrival there, because the potential consequences are considered to be similar for both coasts. As natural, long-distance dispersal of C. intestinalis is unlikely given the short larval period, perhaps as short as 6 – 36 h (Millar, 1952), increased management of human-mediated dispersal vectors could substantially reduce the potential for C. intestinalis to arrive on the Pacific coast (or to spread on both coasts). Secondary spread by recreational watercraft and aquaculture-related transfers have been identified for this species already (Cohen et al., 2000; Lambert and Lambert, 2003), and increased management of these potential vectors could limit spread. Although relatively little information was available on pathogens, parasites, or fellow travellers, the parasite responsible for AGD, Neoparameoba pemaquidensis, has been found on C. intestinalis in Tasmania, and it could pose a problem for salmon aquaculture elsewhere (Tan et al., 2002). Because of the potential ecological consequences of AGD, the overall risk of pathogens, parasites, and fellow travellers of C. intestinalis affecting both coasts was moderate but with great uncertainty. This suggests that potential pathogen issues could be looming, posing increased risk to wild and cultured species. Although data limitations can affect the risk assessment, it helps to identify important areas for future research by identifying data gaps needed to be closed to improve future risk assessments. The overall genetic risk posed by these organisms was determined to be low, again with great uncertainty. Conducting risk assessments for NIS is relatively new, and a range of different approaches has been described. Our overall risk score was based on categorical variables for the probability and consequences of establishment, based on an expert survey and combined using a heat matrix. Similar approaches have been adopted for other risk assessments. For example, Kluza et al. (2006) employed such a methodology to assess an invasive tunicate in New Zealand, and introductions and transfer committees use the approach for intentional introductions (e.g. DFO, 2003). The widely adopted weed risk assessment uses a set of questions that are combined to give an overall numerical score, thereby identifying plants that should be accepted, rejected, or investigated further before being introduced (Pheloung et al., 1999). Relative risk models also exist, such as the one applied to Carcinus maenas (European green crab), where ranked introduction exposure, habitat availability, and impacts on a preselected group of species were combined (Colnar and Landis, 2007). Also, Herborg et al. (2007) developed a relative risk ranking of ports, based on suitability and introduction effort for Eriocheir sinensis (Chinese mitten crab). The advantage of the heat matrix approach used here is the robustness of the approach to data of various qualities, which becomes even more important in datalimited situations. Despite being qualitative, this approach is well suited to situations when rapid evaluation is required, or when data do not allow more quantitative approaches to be used. Considering the limited scientific literature on dispersal pathways and specific impacts, our expert survey provided an important tool for informing the risk assessment. Expert surveys have been used successfully in related areas, such as informing the Australian weed risk assessment model (Pheloung et al., 1999) and management decisions on widespread species of concern (Kometter et al., 2004). Similarly, Nielsen and Scott (1994) demonstrated how expert surveys could be used to direct research and monitoring efforts to priority areas. Nevertheless, survey results have to be studied critically. For example, respondents to our survey who identified themselves as having general tunicate knowledge ranked ballast water transport higher than did respondents with species- or group-specific knowledge, although no group ranked ballast water transport among its top three potential vectors (Table 1). This potential artefact could have arisen because Downloaded from https://academic.oup.com/icesjms/article/65/5/781/714476 by guest on 25 March 2024 Figure 2. Heat matrix showing the ecological (Ecol) or genetic (Gen) risk for either the Atlantic coast (EC) or Pacific coast (WC) of Canada, for Ciona intestinalis (Ci) and for pathogens, parasites, or fellow travellers (FT). 785 786 Acknowledgements This work was supported by funds from DFO’s AIS programme and funds from the Centre of Expertise for Aquatic Risk Assessment (CEARA). We also thank the participants from the Charlottetown, Prince Edward Island, tunicate meeting for helpful advice, comments, and discussion. Three anonymous reviewers provided suggestions that greatly improved the manuscript. References Becheikh, S., Thomas, F., Raibaut, A., and Renaud, F. 1996. Some aspects of the ecology of Pachypygus gibber (Copepoda), an associated organism of Ciona intestinalis (Urochordata). Parasite, 3: 247– 252. Bingham, B. L., and Walters, L. J. 1989. Solitary ascidians as predators of invertebrate larvae: evidence from gut analyses and plankton samples. Journal of Experimental Marine Biology and Ecology, 131: 147 – 159. Blum, J. C., Chang, A. L., Liljesthröm, M., Schenk, M. E., Steinberg, M. K., and Ruiz, G. M. 2007. The non-native ascidian Ciona intestinalis (L.) depresses species richness. Journal of Experimental Marine Biology and Ecology, 342: 5 – 14. Byrd, J., and Lambert, C. C. 2000. Mechanism of the block to hybridization and selfing between the sympatric ascidians Ciona intestinalis and Ciona savignyi. Molecular and Reproductive Development, 55: 109– 116. Carver, C. E., Chisholm, A., and Mallet, A. L. 2003. Strategies to mitigate the impact of Ciona intestinalis (L.) biofouling on shellfish production. Journal of Shellfish Research, 22: 621 – 631. Cohen, B. F., McArthur, M. A., and Parry, G. D. 2000. Exotic marine pests in Westernport. Marine and Freshwater Research Institute Reports, 22. 17 pp. Colnar, A. M., and Landis, W. G. 2007. Conceptual model development for invasive species and a regional risk assessment case study: the European green crab, Carcinus maenas, at Cherry Point, Washington, USA. Human and Ecological Risk Assessment, 13: 120– 155. DFO 2003. National Code on Introductions and Transfers of Aquatic Organisms. 53 pp. www.dfo-mpo.gc.ca/science/aquaculture/ code/Code2003_e.pdf (last accessed 24 December 2007) Dybern, B. I. 1965. The life cycle of Ciona intestinalis (L.) f. typica in relation to the environmental temperature. Oikos, 16: 109– 131. Hayes, K. R. 1998. Ecological risk assessment for ballast water introductions: a suggested approach. ICES Journal of Marine Science, 55: 201– 212. Herborg, L. M., Jerde, C. J., Lodge, D. M., Ruiz, G. M., and MacIsaac, H. J. 2007. Predicting invasion risk using measures of introduction effort and environmental niche model. Ecological Applications, 17: 663– 674. Holt, J. 2006. Score averaging for alien species risk assessment: a probabilistic alternative. Journal of Environmental Management, 81: 58 – 62. Keller, C., Siegrist, M., and Gutscher, H. 2006. The role of the affect and availability heuristics in risk communication. Risk Analysis, 26: 631– 639. Kluza, D., Ridgway, I., Kleeman, S., and Gould, B. 2006. Organism Impact Assessment: Styela clava (Clubbed Tunicate). Biosecurity New Zealand. 19 pp. Kometter, R. F., Martinez, M., Blundell, A. G., Gullison, R. E., Steininger, M. K., and Rice, R. E. 2004. Impacts of unsustainable mahogany logging in Bolivia and Peru. Ecology and Society, 9: 12 – 31. Kott, P. 1990. The Australian Ascidacea. 2, Aplousobranchia. Memoirs of the Queensland Museum, 29(10). 298 pp. Lamb, A., and Hanby, B. P. 2006. Marine Life of the Pacific Northwest: a Photographic Encyclopedia. Harbour Publishing, Madeira Park, BC. 398 pp. Lambert, C. C., and Lambert, G. 2003. Persistence and differential distribution of nonindigenous ascidians in harbors of the Southern California Bight. Marine Ecology Progress Series, 259: 145 – 161. Locke, A., Hanson, J. M., Ellis, K. M., Thompson, J., and Rochette, R. 2007. Invasion of the southern Gulf of St Lawrence by the clubbed tunicate (Styela clava Herdman): potential mechanisms for invasion of Prince Edward Island estuaries. Journal of Experimental Marine Biology and Ecology, 342: 69 – 77. Lockwood, J. L., Cassey, P., and Blackburn, T. 2005. The role of propagule pressure in explaining species invasions. Trends in Ecology and Evolution, 20: 223– 228. McDonald, J. H., Seed, R., and Koehn, R. K. 1991. Allozymes and morphometric characters of three species of Mytilus in the northern and southern hemispheres. Marine Biology, 111: 323 – 333. Millar, R. H. 1952. The annual growth and reproduction in four ascidians. Journal of the Marine Biological Association of the UK, 31: 41 – 61. Millar, R. H. 1966. Ascidiaceae. Scandinavian University Books, Oslo. 123 pp. Millar, R. H. 1971. The biology of ascidians. Advances in Marine Biology, 9: 1 – 100. Nielsen, L. A., and Scott, M. T. 1994. An expert survey of information needs for Ohio sport and commercial fishes. Ohio Journal of Science, 94: 55– 59. NIMPIS 2002. Ciona intestinalis species summary. National Introduced Marine Pest Information System. Ed. by C. L. Hewitt, R. B. Martin, C. Sliwa, F. R. McEnnulty, N. E. Murphy, T. Jones, and S. Cooper http://crimp.marine.csiro.au/nimpis (last accessed 24 December 2007). Downloaded from https://academic.oup.com/icesjms/article/65/5/781/714476 by guest on 25 March 2024 of the role of affect in risk communication (Keller et al., 2006), ballast water having been implicated in a number of high-profile introductions. Therefore, respondents to our survey with less knowledge of tunicates consider this vector relatively important, without recognizing that life-history characteristics of the species would limit their use of this vector. However, all three groups identified aquaculture-related transfers and slow-moving vessels as higher risk vectors, suggesting that expert solicitation is useful and can be informative, especially when published information is limited. Risk assessments are a starting point, meant to be used as a basis for decision-makers, managers, and policy-makers who have to manage, control, or mitigate the potential impact of NIS. Moreover, biological risk assessments are only one component of an overall risk analysis framework, which should include a socio-economic risk assessment. It should be expected that risk assessments will need to be revisited from time to time as more information is gained and data gaps filled. Given the recently increasing concern about the potential risks posed by non-indigenous tunicate species in marine waters, there are a number of areas where basic information is lacking, making risk assessment more difficult. This is especially true where greater levels of uncertainty have been identified, such as those associated with pathogens, parasites, and fellow travellers. Also, for organisms not already established and spreading, additional qualification of arrival potential would be necessary, for example, combining the vector importance ranking determined from the survey with actual vector data (e.g. vessel arrivals, ballast water discharge, number of aquaculture-related movements). Although it may never be possible to predict an invasion, risk assessments are obviously vital to inform the decision-making process. T. W. Therriault and L-M. Herborg 787 Qualitative biological risk assessment for Ciona intestinalis in Canada Appendix Vector importance Very low: tunicates have not been demonstrated or believed to utilize this vector; does not require management. Low: tunicates are unlikely to spread by this vector; may require effort to minimize spread. Moderate: tunicates can spread by this vector in favourable circumstances; management could reduce spread. High: tunicates have used this vector extensively; management would be important in reducing spread, but has not been attempted. Very high: tunicates have used this vector extensively despite extensive management effort. Vector uncertainty level Very high uncertainty: little or no information; expert opinion based on general species knowledge. High uncertainty: limited information; third party observational information or circumstantial evidence. Moderate uncertainty: moderate level of information; first hand, unsystematic observations. Low uncertainty: substantial scientific information; non-peerreviewed information. Very low uncertainty: extensive scientific information; peerreviewed information. Potential impact level Positive: Positive impact; improvement of the factor in question. Very low (negative): no measurable impact; consequences can be absorbed without additional management action. Low (negative): measurable, limited impact; disruption to the factor in question, but reversible or limited in time, space, or severity; may require management effort to minimize it. Moderate (negative): measurable, widespread impact; widespread disruption to the factor in question, but reversible, or of limited severity, or duration; can be managed under normal circumstances. High (negative): significant impact; widespread disruption to the factor in question that persists over time, or is likely irreversible; will require effective management or adaptation of procedures. Very high (negative): critical impact; extensive disruption to the factor in question, which is irreversible; may already be unmanageable, or will become so unless effective management is immediately put in place. Impact uncertainty levels Unlikely: impact only under exceptional circumstances, or not expected. Possible: impact possible under some circumstances. Likely: impact probable under most circumstances. Almost certain: impact expected under most circumstances. Certain: impact already observed. doi:10.1093/icesjms/fsn059 Downloaded from https://academic.oup.com/icesjms/article/65/5/781/714476 by guest on 25 March 2024 Ooishi, S., and O’Reilly, M. G. 2004. 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Journal of Environmental Management, 57: 239– 251. Ramsay, A., Davidson, J., Landry, T., and Arsenault, G. Process of invasiveness among exotic tunicates in Prince Edward Island, Canada. Biological Invasions (in press). Ruiz, G. M., Fofonoff, P. W., Carlton, J. T., Wonham, M., and Hines, A. H. 2000. Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annual Review of Ecology and Systematics, 31: 481 – 531. Sala, O. E., Chapin, F. S., Armesto, J. J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., et al. 2000. Global biodiversity scenarios for the year 2100. Science, 287: 1770– 1774. Tan, C. K. F., Nowak, B. F., and Hodson, S. L. 2002. Biofouling as a reservoir of Neoparamoeba pemaquidensis (Page, 1970), the causative agent of amoebic gill disease in Atlantic salmon. Aquaculture, 210: 49 – 58. Therriault, T. W., and Herborg, L-M. 2008. 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