A comparison of eight country plans for the Invasive Indo-Pacific Lionfish in the Wider Caribbean

Global Ecology and Conservation 12 (2017) 253e262

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Original Research Article

A comparison of eight country plans for the Invasive Indo-Pacific Lionfish in the Wider Caribbean Roxanne E. Graham, Lucia M. Fanning* Marine Affairs Program, Life Sciences Centre, Dalhousie University, Room 800, 1355 Oxford Street, PO Box 15000, Halifax Nova Scotia B3H 4R2, Canada

a r t i c l e i n f o

a b s t r a c t

Article history: Received 27 October 2017 Received in revised form 4 December 2017 Accepted 4 December 2017

The effects of climate change and marine invasive species have posed a major threat to significant ecological, aesthetic, economic and amenity value to the countries and territories of the Wider Caribbean Region. Today, the Caribbean Sea is plagued with the invasive lionfish (Pterois volitans and P. miles). As the range and abundance of the lionfish throughout the Caribbean has grown, recognition of the grave threat it poses to the native marine ecosystems has prompted the development of lionfish management plans across the region. The efforts of eight countries in the region to manage lionfish are evaluated using the US Environmental Protection Agency Aquatic Invasive Species framework and the inclusion of climate change and/or changing conditions. The countries and overseas territories evaluated were Anguilla, Bahamas, Cayman Islands, Grenada, St. Eustatius, St. Lucia, St. Vincent and the US Virgin Islands. Although specific strategies differed amongst the islands depending upon needs, culture, and individual circumstances, most of the plans included aspects of education and outreach, control and monitoring protocols, and research and information management. Areas that were found to be notably weak to nonexistent included leadership, prevention, early detection and rapid response and restoration; This comparative analysis provides opportunities for knowledge sharing and intra- and inter-country cooperation, facilitating the transfer and development of interventions that contribute to the conservation of significant island biodiversity. © 2017 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Keywords: Wider Caribbean Region Aquatic invasive species Lionfish management Adaptive capacity

1. Introduction Aquatic Invasive Species (AIS), particularly those in the marine environment, is an issue rapidly increasing in importance and relevance in the Caribbean but thus far, little has been done to address the problem through marine planning and management (Kling and Sanchirico, 2014). As nations become more interdependent and trade continues to flourish, the problem of invasions, defined as species that are not origin to a given region, is becoming more difficult to handle (Kannan, 2015). The current scientific discourse suggests that invasive species, “due to their lack of co-evolutionary history with the native environment” (Simberloff, 2005), may cause significant ecological impacts on native species and their habitat, leading to economic and social impacts for communities that depend on these resources. Some of these negative effects include displacement of native species, loss of native genotypes, changes in community structure, foodweb properties, ecosystem

* Corresponding author. E-mail addresses: [email protected] (R.E. Graham), [email protected] (L.M. Fanning). https://doi.org/10.1016/j.gecco.2017.12.001 2351-9894/© 2017 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/).

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rdenas, 2015; processes and services, impacts on human health, and the potential for substantial economic losses (Carballo-Ca Katsanevakis et al., 2014; Layman and Allgeier, 2012). Despite an increased awareness of invasion problems in the scientific community, national governments continue to fall short on implementing preventative measures to detect or counteract their emergence, tending more towards reactive policies aimed at managing invasive species that are already established and problematic (Early et al., 2016; Kannan, 2015). In terms of response management, marine environments present exceptionally challenging conditions for the control of bio-invasions due to the absence of clear borders which severe limits management options in three dimensions (Lopez and Krauss, 2006). One such invasion and corresponding need for improved response management has recently unfolded in the Wider ^te
et al. (2013), it is at a rate and Caribbean Region (WCR) (Albins, 2016; Andradi-Brown et al., 2017). According to Co magnitude never before documented in any marine system. It involves two species of Indo-Pacific lionfish (Pterois volitans and P. miles), which represent the first non-native marine finfish to become established in the Atlantic waters of the United States, including the Gulf of Mexico and Caribbean (ANSTF, 2015). The resulting impacts of the invasion in the WCR have been ecological, economic and social. As an invasive species to the Caribbean, the lionfish, with no known predator, voracious appetites and high rates of reproduction, has the competitive advantage over native species (Albins, 2013; Lesser and Slattery, 2011; Kulbicki et al., 2012; Rocha et al., 2015; Simmons, 2014). Lionfish abundance increased rapidly between 2004 and 2010 in the Atlantic Ocean and Caribbean Sea (Green et al., 2012). By 2010, lionfish comprised nearly 40% of the total predator biomass in the system, coinciding with a 65% decline in the biomass of the lionfish's 42 Atlantic prey fishes in just two years (Green et al., 2012). Additionally, lionfish have been found to have reduced the abundance of small native reef fishes by up to 95% at some invaded ^te
et al., 2013) while some studies have found no measurable effect on prey fish community structure (Hackerott sites (Co et al., 2017). Economically, in addition to preying on or outcompeting commercially valuable species leading to a decrease in the economies of fishing communities (Ballew et al., 2016), lionfish may also impact the recreational sector and local tourism due to a perceived absence of attractive game and reef cleaning species (Morris and Whitfield, 2009). From a human health perspective, an increasing concern is the capacity for lionfish to inject neurotoxins dangerous to humans (and other animals) from stout spines on several of the main fins, requiring immediate professional medical evaluation and treatment (Haddad et al., 2015). Given these diversity of issues needing to be addressed, management and control actions of lionfish have been challenging at best (Bratspies, 2013; Hackerott et al., 2017; Morris, 2012; Peiffer et al., 2017). While there is a Regional Strategy for the
mez Lozano et al., 2013), it lacks an assessment and evaluation tool to Control of Invasive Lionfish in the Wider Caribbean (Go guide and report on collaboration. Efforts have been localized and not well coordinated across agencies or with other stakeholders (ANSTF, 2015). Additionally, climate change has been shown to benefit some marine invasive species due to range shifts and competition effects (U.S. Environmental Protection Agency (EPA), 2008). For lionfish, research has illustrated the possible correlation between temperature rise and their spread. Small changes of 1
C in winter bottom water temperatures have already shifted the species balance in some marine ecosystems from tropical towards temperate communities (Burgiel and Muir, 2010; Figueira and Booth, 2010). The aim of this research is to provide a comprehensive perspective on localized and regional lionfish management practices and challenges in the Caribbean and to determine their adaptive capacity to adjust to climate change and other changing conditions. It does this by conducting a comparative analysis of lionfish management plans in eight islands in the WCR. The countries evaluated were Anguilla, Bahamas, Cayman Islands, Grenada, St. Eustatius, St. Lucia, St. Vincent and the US Virgin Islands. We provide an assessment of the management activities for lionfish control in the Wider Caribbean, and analyze each of the selected country plans for adaptive capacity under possible changing conditions. We also identify opportunities and obstacles to enhancing the Caribbean's current approach to managing the invasive lionfish. 2. Method The countries in this study were selected on the basis of the accessibility and availability of country plans. Due to time and language restrictions, case studies for analysis were limited to English-speaking countries in the Caribbean with lionfish management plans. Documentation on the plans for the eight countries and territories used in the study included both those provided by relevant national informants and those available on the internet. Wherever possible, currency of the plans was confirmed by national informants attached to the relevant institution or government department. National informants also shared detailed information on some of the management practices that were lacking in the plan and provided needed clarification to questions from the researchers. The analytical framework used to assess the responsiveness of the management plans was the US Environmental Protection Agency (USEPA) Aquatic Invasive Species (AIS) Management Framework (Premo et al., 2014). Despite the geopolitical differences of the countries within the WCR, most effective regional plans associated with coastal and marine management use a strategic management framework (Department of Fisheries and Oceans Canada (DFO), 2004) and offer specific guidance and assessment tools to ensure countries are addressing key aspects of management (Halpern et al., 2012). Since the USEPA AIS Management Framework is the standard and leading example of a framework used for assessing AIS management performance in states and territories within the US, including those in the Caribbean (Premo et al., 2014), we decided to use it as our reference guide. We acknowledge the similarity between this framework and the Wider Caribbean Regional Strategy

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Table 1 Assessment of management activities in Country plans. Country

Leadership & Coordination

Prevention EDRR Control & Management

Restoration Research Information Management

Education & Awareness

Total

Anguilla Bahamas Cayman Islands Grenada St. Eustatius St. Lucia St. Vincent USVI

1 2 3

0 0 0

0 0 0

1 2 3

0 0 0

1 2 3

1 3 1

2 3 3

5 12 13

3 2 2 1 3

0 0 0 0 3

1 1 0 1 1

2 2 1 2 2

0 0 0 0 0

0 2 1 3 3

1 2 1 1 2

3 3 3 2 3

10 12 8 10 17

Scoring: 0 ¼ not addressed; 1 ¼ implicitly addressed (i.e. includes goals and strategies that may be used to account for the activities); 2 ¼ explicitly addressed but not linked to any associated goals and/or action items; 3 ¼ yes, explicitly addressed and specifies associated goals and/or action items.

for the Control of the Invasive Lionfish.1 However, we opted for the USEPA Aquatic Invasive Species Management Framework as its management activities and categories included four additional factors (identified in italics) that were lacking in the Caribbean Regional Strategy: leadership and coordination; prevention; early detection and rapid response; restoration; control and management; research; information management; and education and public awareness (National Invasive Species Council, 2001). The assessment of performance of country plans was based on a scoring system where 0 ¼ not addressed; 1 ¼ implicitly addressed (i.e. includes goals and strategies that may be used to account for the activities); 2 ¼ explicitly addressed but not linked to any associated goals and/or action items; 3 ¼ explicitly addressed and specifies associated goals and/or action items. Additionally, the following criteria were also evaluated for each of the eight country plans using a scoring system specific to the issue being assessed (details provided in Tables 2e6): i. ii. iii. iv. v.

Capacity to adapt goals and activities to changing conditions Potential impacts resulting from climate change Provision of monitoring strategies Plans for periodic revision and update of the plan Description of funding sources/strategies for plan implementation.

3. Results 3.1. Assessing management activities in country plans As shown in Table 1, each plan had some level of activities focusing on management and control, education and awareness and provided evidence of organization with regards to leadership and coordination. In contrast, most plans did not specify any form of prevention, whether in the form of addressing new introductions, increasing growth, impacts on native species that are economically and ecologically viable or endangerment to public health and safety. Only the USVI plan clearly acknowledged the prevention of increasing populations by having specific monitoring sites. Early detection and rapid response (EDRR) seems to be non-existent or hardly acknowledged in the eight country plans. While Grenada, St. Eustatius and USVI implicitly addressed rapid response and removal as it relates to the lionfish, only St. Vincent additionally included the need for EDRR for potentially new introductions of similar invasive species. None of the country plans accounted for restoration. This is not a surprise as most Caribbean countries lack information on the status of their marine ecosystem and the degree to which negative impacts upon marine biodiversity is due solely to the lionfish (Miloslavich et al., 2010). According to these authors, despite a long history of scientific research in the region, the present knowledge about Caribbean marine biodiversity and species distribution does not satisfy the needs for objectively defining geographic conservation priorities and designing management plans at a regional scale. 3.2. Similarities and differences in the level of activities among pairs of countries A visual illustration of the similarities and differences in the level of management activities among pairs of countries is provided in Fig. 1, where “hotter” colors (e.g., red, orange and yellow) correspond to more problematic situations, i.e., no activity is the worst possible situation (red), no match is the second worst situation (orange), different stages of development is problematic but not fatal (yellow), and matching is the goal (green). Overall, there are comparatively more yellow boxes

1
mez Lozano et al., in 2013, published the Regional Strategy for the Control of Invasive Lionfish in the Wider Caribbean. The strategy aims to establish Go a framework for action for Caribbean countries to prevent, minimize and mitigate the adverse impacts of the lionfish on biodiversity and ecosystem services, as well as limiting social and economic damage.

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Table 2 Capacity of planned activities to adapt to changing conditions. Country

Leadership & Coordination

Prevention EDRR Control & Management

Restoration Research Information Management

Education & Awareness

Total

Anguilla Bahamas Cayman Islands Grenada St. Eustatius St. Lucia St. Vincent USVI

0 1 0

0 0 0

0 0 0

1 3 1

0 0 0

1 1 0

0 1 1

1 1 1

3 7 3

1 1 0 0 1

0 1 0 0 1

1 1 0 1 1

1 2 0 2 1

0 0 0 0 0

0 1 1 1 1

0 1 1 1 1

1 1 1 1 2

4 8 3 6 8

Scoring: 0 ¼ not addressed; 1 ¼ implicitly addressed (i.e. includes goals and strategies that may be used to account for changing conditions as part of their purpose); 2 ¼ explicitly addressed but not linked to any associated goals and/or action items to account for changing conditions; 3 ¼ yes, explicitly addressed and specifies associated goals and/or action items to account for changing conditions.

Table 3 Incorporation of potential impacts resulting from climate change. Country

Total Plan acknowledges climatic Plan demonstrates understanding Plan identifies research on the Plan specifically potential effects of species responding mentions climate boundaries of species (zones) of species and/or ecosystem sensitivity to changing conditions to changing conditions change

Anguilla Bahamas Cayman Islands Grenada St. Lucia St. Eustatius St. Vincent USVI

1 0 0 1 0 0 0 0

2 2 2 2 1 2 1 2

2 1 0 2 0 1 1 2

1 1 0 0 0 2 1 0

6 5 2 5 1 5 4 4

Scoring: 0 ¼ not addressed; 1 ¼ brief mention of issue in the plan; 2 ¼ general discussion of issue in the plan; 3 ¼ discussion of issue includes quantitative information and/or specific examples in the plan.

Table 4 Monitoring strategies. Country

Plan includes strategy for changing conditions

Plan includes strategy to utilize monitoring data

Plan includes strategy for managing/updating monitoring data

Total

Anguilla Bahamas Cayman Islands Grenada St. Eustatius St. Lucia St. Vincent USVI

0 0 0

0 1 1

0 1 3

0 2 4

0 0 0 0 1

1 1 1 1 1

0 1 1 1 3

1 2 2 3 5

Scoring: 0 ¼ not addressed; 1 ¼ brief mention of issue in the plan; 2 ¼ general discussion of issue in the plan but unclear how information will be used; 3 ¼ discussion of issue with clarity around use of information in the plan.

Table 5 Periodic revision and update. Country

Plan includes strategy for updating and incorporating new information

Anguilla Bahamas Cayman Islands Grenada St. Eustatius St. Lucia St. Vincent USVI

1 1 1 0 1 1 1 1

Scoring: 0 ¼ not addressed; 1 ¼ brief mention of issue in the plan; 2 ¼ general discussion of issue in the plan; 3 ¼ discussion of issue with timeline and/or benchmarks provided.

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Table 6 Country assessment relating to funding sources/strategies for plan implementation. Country

Score

Anguilla Bahamas Cayman Islands Grenada St. Eustatius Saint. Lucia St. Vincent & the Grenadines USVI

3 2 1 3 0 3 0 2

Scoring: 0 ¼ not addressed; 1 ¼ a source is specified for a portion of the required funding; 2 ¼ a source is specified for a portion of the required funding along with strategies for obtaining remaining funding; 3 ¼ a source is specified for 100% of the required funding.

Fig. 1. Comparison of set of management activities for the invasive lionfish among case study countries. Legend: Red Boxes e No activity in either country; Orange boxes - No Match (no activity in one country vs. some activity in other country); Yellow boxes e Different Match (activities at different stages in the two countries); Green boxes - Complete Match (activities at similar stage in both countries). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

than other colors, suggesting that across the studied countries, planning and expected outcomes for management of the lionfish were occurring but inconsistent among the pairs of countries being assessed. However, it also suggests that, given the evidence of the levels of activity in the plans being compared, improvements in the category by the country with the lower level could be possible through sharing of expertise and practice from the country at the more advanced stage of the activity. Areas in need of attention among all countries include efforts targeting restoration, followed by prevention. In Anguilla, the Bahamas and Cayman Islands, EDRR activities were also flagged as needing attention. In contrast, Education and Awareness, Information Management and Leadership and Coordination were three activities having the most attention being paid to by pairs of countries assessed. An integrated assessment of the results for all eight countries highlights opportunities for collaborative improvement in invasive species management among these countries in the WCR. 3.3. Assessing adaptive capacity for changing conditions in country plans Tables 2e6 illustrate each country's plan with respect to how well it: (1) demonstrated capacity to adapt goals and activities to changing conditions, (2) addressed potential impacts resulting from climate change, (3) provided monitoring strategies, (4) included plans for periodic revision and updating, and (5) described funding sources/strategies for plan implementation. While most country plans did not mention climate change or changing conditions, the assessment showed some capacity for countries to adapt their program's goals or activities (Table 2). However, each category had some level of changing conditions needing to be considered. For example, leaders and coordinating bodies in AIS related projects should be aware of changing conditions as it relates to sensitive reef ecosystems and species of conservation concerns, to name a few. According to U.S. Environmental Protection Agency (EPA) (2008), this enables managers and decision-makers to experience less difficulty in addressing potential program vulnerabilities to climate change. The results illustrate that countries that scored high in their planned management activities for lionfish such as the USVI and Cayman Islands (Table 1), scored considerably lower when incorporating adaptive capacity for changing conditions in the performance assessment (Table 2). The results of Table 3 illustrate the level in which each plan incorporated potential impacts resulting from climate change. Out of a possible score of 12, Anguilla scored the highest, achieving a score of 6. The findings suggest that the majority of country plans have management actions that may prove less relevant, less efficient, or less successful under a changing climate scenario than they are under current conditions (U.S. Environmental Protection Agency (EPA), 2008). There is clearly a

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need for countries in the region to better incorporate climate change data in their plans. Cayman Islands and St. Lucia are two countries which scored very poorly in this assessment. As it relates to monitoring strategies (Table 4), seven of the eight countries (excepting Anguilla) had clear strategies for using the data. Furthermore, only Anguilla and Grenada did not allow for managing and updating monitoring data. Monitoring objectives were largely proposed for number of caught lionfish and key native fish species populations. The USVI plan received the highest ranking with a score of five out of a total of nine points. The objectives of an updated USVI plan included collaboration on research and monitoring, data gathering and analysis to improve understanding of lionfish impacts, effectiveness of removal and examining the local and regional scientific research with observational data and by concentrating the collection of removal and sighting data into one shared database (Kilgo, 2014). Seven of the eight country plans (excepting Grenada) implicitly included periodic revisions and updating of information (Table 5), recognizing the need to include new information and update goals and activities. According to U.S. Environmental Protection Agency (EPA) (2008), the identification of funding indicates an overall high capacity for states to accomplish tasks in management plans. Six of the eight country plans, excluding St. Eustatius and St. Vincent, had some level of funding stated or a strategy to acquire funding, (Table 6). However, the analysis of all country plans suggested that much of the funding is dedicated principally to education and public awareness at the expense of other important components of a successful management plan. Financial resources need to be sourced and allocated to all components of the AIS plan at national and regional levels to accomplish the objectives and goals associated with managing lionfish in the Caribbean. The scores from tables two through six are accumulated and illustrated in Fig. 2. The best possible score is 51 and none of the countries scored even half of this total. This clearly illustrates a need for improving the plans by revisiting weak areas and incorporating climate and/or changing conditions. Not surprising, the USVI, score is the highest, likely because it is a US territory and is being guided by the National Invasive Species Council (2001) and assessed under the US EPA AIS framework (2008).

4. Discussion Many of the strategies required to deal with the threat of AIS call for action within a specific pathway or with respect to a single species (Department of Fisheries and Oceans Canada (DFO), 2016). This is encouraging for managers in the case study

Fig. 2. Overall adaptive capacity assessment for changing conditions in AIS management plans in case study countries (maximum score ¼ 51).

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countries since the existing lionfish plans are specific to this species. However, the analysis of the eight plans against the criteria recommended by the USEPA-AIS Management Framework suggests that there is considerable room for improvement, given the scope of the problem combined with its continued growth if left unchecked. Focused efforts on the management of AIS are a relatively recent phenomenon in the WCR and collaborative, transboundary management remains a major challenge to the conservation of marine ecosystems in the region (Fanning et al., 2011). In contrast with terrestrial invasions, government and other actors have been slow to recognize marine introductions as an issue, primarily due to a lack of information and demonstrable impacts to human health, ecosystems, and economies (Hewitt et al., 2009). However, there is an increasing recognition that a lack of collaboration between states often produces harmful socioecological consequences and efforts are being made to address this gap in governance (Debels et al., 2017). Management planning with common goals is an important first step for a unified and cooperative approach to addressing invasive species issues (National Invasive Species Council, 2001). Based on the findings of this study, we suggest that the Wider Caribbean Regional Strategy for the Control of Invasive Lionfish needs to be revised and formally endorsed by countries in the region to include an assessment framework drawing on the 2008 US EPA AIS framework. Such an endorsement should also ensure the necessary local and regional regulatory and legislative instruments and authority are in place. It should also allow for increased partnership building, a clear framework for cooperation among partners and sustainable funding sources for long-term implementation of AIS strategies at both the national and regional level. In general, collaboration and coordination are themes that flow throughout the AIS management plans discussed in this paper. Additionally, the research underscores the need to consider climate-change effects in every part of AIS management plans and programs in order to address AIS effectively. According to Mohammed (2016), one of the eleven specific recommendations for improving implementation of the Caribbean Regional Lionfish Strategy is to review existing policy and legislation, with the proposed amendments being general enough to address current issues as well as issues likely to arise in the near future. Existing AIS related plans in the Caribbean are actually in various stages of both development and implementation, and some countries operate a multitude of AIS management activities and programs in the absence of an articulated plan. However, the results of this comparative analysis, as focused on the eight categories identified in the US EPA AIS Assessment Framework, may provide guidance on gaps and opportunities for enhancing efforts to manage marine invasive species such as the lionfish.

4.1. Gaps and opportunities 4.1.1. Leadership and coordination The results indicated that country plans had varying degrees of organization regarding leadership and coordination (Table 1). Plans scoring low lacked a responsible entity and coordinated system for management actions. As AIS response in the WCR
mez Lozano et al., 2013), inter-sectoral commitment from numerous departments and is largely inter-governmental (Go agencies across all levels of government as well as other stakeholders is essential. In the current absence of a functioning regional body to coordinate the overarching policy integration and coordination role for ocean affairs in the WCR (Debels et al., 2017), national governments and relevant regional and international intergovernmental bodies such as the United Nations Environment Programme e Caribbean Environment Programme (UNEP-CEP) need to commit to providing the necessary leadership and enhance collaborative solutions to the lionfish threat and potential future threats, at both the national and regional level. 4.1.2. Prevention Our results indicate the near absence of preventative efforts in the country plans examined. Generally, the most costeffective way to reduce impacts of invasive species is to prevent them from establishing in the first place (Harvey and Mazzotti, 2014). However, given the existence of numerous anthropogenic (e.g. the Panama Canal serving as a major global maritime corridor for ships transiting the region) and natural pathways that increase the likelihood of introductions (e.g. hurricanes, ocean currents, warming sea temperatures), it may be more effective for strategies and actions specific to lionfish to focus on monitoring, detecting, and response rather than prevention (Bratspies, 2013; Johnston and Purkis, 2015; Schofield, 2010). 4.1.3. Early Detection and Rapid Response (EDRR) Half of all country plans reviewed did not include any activities for EDRR nor did they mention a need for it (Table 1). This is likely due to inadequate planning, jurisdictional issues, insufficient resources and authorities, limited technology, and other factors which often hamper early detection and rapid response in many locations, including the WCR (Waugh, 2009). There was also no mention in the Caribbean regional strategy that a comprehensive regional system was in place for detecting and responding to incipient invasions. Given the enormous number of known AIS and the unknown number of AIS yet to emerge, rapid evaluation schemes to prioritize responses appear to be a significant gap in the region that need to be filled. This can be achieved through improved marine environmental monitoring so that newly introduced organisms can be detected and eradicated before they become established. However, implementing an integrated approach to EDRR in the region will require

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agreement on appropriate surveillance programs and responses as well as availability of funds at both the regional and national levels. 4.1.4. Control and management The control techniques being used by countries in the WCR such as culling are proposed to be effective, economical, safe, and targeted to an individual AIS - the lionfish. Control in this case implies that populations of the AIS are declining or are at levels where they can be managed. However, according to research, lionfish populations are currently increasing and are achieving high population densities, reaching well over 400 lionfish per hectare and becoming one of the most abundant species on some reefs (ANSTF, 2015). Based on our analysis, this can be a result of some countries lacking management, thereby undermining the efforts of those that do. Other ways to improve the control status include maximizing the efficiency of existing resources to share information, technologies, and technical capacity such as size of infestation, demonstrated history of successful control elsewhere, knowledge of species life history, potential environmental impact, likelihood of reintroduction and the availability of approved control tools among countries in the region (Tahoe Regional Planning Agency (TRPA), 2014). Additionally, we recommend that intergovernmental bodies and existing organisation and entities such as the Caribbean Oceanic Restoration and Education Foundation (CORE) could examine and where feasible, implement legal policies to regulate the aquarium trade of finfish and other potential exotic marine species, as well as conditions and gear for lionfish removal. 4.1.5. Restoration Consistent with guidance in the USEPA AIS Management Framework (2008), strategies for addressing AIS advocate restoration. However, none of the case study countries addressed this criterion. This oversight could result in a delay in damaged ecosystems regenerating themselves and an increased susceptibility to subsequent invasions, even if efforts to decrease lionfish populations are successful (Department of Fisheries and Oceans Canada (DFO), 2004). For the Caribbean, restoration may involve taking an active approach in terms of encouraging native species to thrive, such as reducing fishing pressure on the commonly fished stocks (e.g. parrot fish) that are in decline (Perry et al., 2013). 4.1.6. Research Research supporting management plans for the lionfish within the WCR fluctuated among the countries. This may be explained by competing or low priorities being given for research and monitoring during the implementation phase of the plans as well as funding and technical capacity. Current research efforts in the Cayman Island and USVI include evaluating the effectiveness of physical removal methods such as diver-assisted sanctions and monitoring lionfish distribution. Additionally, departments in the US engaged in invasive species prevention and control activities have developed a variety of databases and decision support tools to increase predictive capacity for preventing introduction of new invasive species and to improve control efforts (National Invasive Species Council, 2001). Given earlier comments on prevention, we recommend that priority should be given first to improve lionfish control efforts at the national and regional level in the WCR by accessing such databases and decision support tools. 4.1.7. Information management Only the Bahamas scored high for the category of information management (Table 1), providing a detailed account of their arrangements for managing and use of information and involvement of stakeholders. Mention must also be given to the USVI's Caribbean Oceanic Restoration and Education Foundation (CORE) monitoring system, known as the ‘lionfish response hotlines’. CORE developed an online lionfish sighting and removals reporting form and map that can be used to help track control efforts (Kilgo, 2014). For managers that are considering introducing or developing information management systems as stated in some of the country plans, we recommend consideration be given to the U.S. Environmental Protection Agency (EPA) (2008) suggestions for countries in the WCR to develop one that will support rapid and accurate discovery of data, correlate and synthesize data from many sources, and present results of data synthesis that meets the needs of users. 4.1.8. Education and public awareness The results for education and public awareness revealed that 75% of the Caribbean countries analyzed in this study have strong educational and awareness strategies. Most educational program goals have common themes which are to increase public awareness on identifying the lionfish, how to properly capture it, understanding its negative impacts, what to do if stung and promoting lionfish consumption. The management plans also captured similar campaign slogans including but not limited to “Save our reefs, eat lionfish,” “Eat it to Beat it,” “Feast on the Beast” and many more (Carballo-C
ardenas, 2015). Programs to educate the public about the impacts of AIS, methods to prevent introduction and further spread in the region, and control efforts are actively underway by several organizations as well. We suggest ongoing support for such efforts be continued as they play a valuable role in increasing public awareness and engagement in marine conservation (Malpica-Cruz et al., 2016). 5. Conclusion As an invasive finfish species in the western Atlantic Ocean and Caribbean Sea, lionfish have the potential to add additional stress to an environment already compromised by overfishing, pollution and habitat degradation under changing climatic

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conditions (Mahon et al., 2014). Analysis of efforts among the case study countries reveals a multitude of AIS management activities and programs. Despite this, the range of programs designed to control the lionfish, the number of lionfish and their impacts in the Caribbean region are accelerating. In part, we attribute this to the absence or limited attention being paid to key factors in national AIS plans, given the relatively poor performance of the case study country plans when assessed against an accepted AIS management framework standard. However, our analysis also identified a number of opportunities available to mitigate the negative consequences of lionfish in the region. These primarily focused on collaboration and sharing of technical and financial resources, allowing for synergies to be maximized, experiences and failures to be shared and answers to common problems to be identified. With increasing demand for foreign products (Walters and Jones, 2012), increased shipping and cruise tourism, former methods of dealing with invasive species are clearly no longer adequate. By adopting a comprehensive regional framework that guides the development, implementation and assessment of national plans to address lionfish invasion, the destructive consequences of the lionfish and potentially like invasions can be minimized.

Acknowledgement This work was supported by the Canada Queen Elizabeth II Diamond Jubilee Scholarship Program. We also thank all those from the case study countries who provided clarification and additional information on their country's efforts to manage lionfish.

References Albins, M.A., 2013. Effects of invasive pacific red lionfish Pterois Volitans versus a native predator on bahamian coral-reef fish communities. Biol. Invasions 15 (1), 29e43. Albins, M.A., 2016. Behaviours of pacific lionfish facilitate invasion of the atlantic. Biol. Invasions Animal Behav. 309.
gnier-McKellar, C., Jones, O.P., Arteaga, M., 2017. DepthAndradi-Brown, D.A., Grey, R., Hendrix, A., Hitchner, D., Hunt, C.L., Gress, E., Madej, K., Parry, R.L., Re dependent effects of cullingddo mesophotic lionfish populations undermine current management? R. Soc. Open Sci. 4 (5), 170027. ANSTF, 2015. National Invasive Lionfish Prevention and Management Plan. https://www.anstaskforce.gov/Documents/Lionfish_Plan-Final_Approved.pdf. Ballew, N.G., Bacheler, N.M., Kellison, G.T., Schueller, A.M., 2016. Invasive lionfish reduce native fish abundance on a regional scale. Sci. Rep. 6. Bratspies, R.M., 2013. Lionfish as a metaphor for governance in an era of climate change. Nyl. Sch. L. Rev. 58, 829. Burgiel, S.W., Muir, A.A., 2010. Invasive Species, Climate Change and Ecosystem-Based Adaptation: Addressing Multiple Drivers of Global Change. Global Invasive Species Programme (GISP), Washington, DC, US, and Nairobi, Kenya. https://www.gisp.org/whatsnew/docs/Climate_Change_ReportA4.pdf.
rdenas, E., 2015. Controversies and consensus on the lionfish invasion in the western Atlantic Ocean. Ecol. Soc. 20 (3). https://doi.org/10.5751/ Carballo-Ca ES-07726-200324. ^ te
, I.M., Green, S.J., Hixon, M.A., 2013. Predatory fish invaders: insights from Indo-Pacific lionfish in the western Atlantic and Caribbean. Biol. Conserv. 164, Co 50e61. Debels, P., Fanning, L., Mahon, R., McConney, P., Walker, L., Bahri, T., Haughton, M., McDonald, K., Perez, M., Singh-Renton, S., Toro, C., 2017. The CLMEþ strategic action Programme: an ecosystems approach for assessing and managing the caribbean sea and north Brazil shelf large marine ecosystems. Environ. Dev. 22, 191e205. Department of Fisheries and Oceans Canada (DFO), 2004. A Canadian Action Plan to Address the Threat of Aquatic Invasive Species. Canadian Council of Fisheries and Aquaculture Ministers Aquatic Invasive Species Task Group. Department of Fisheries and Oceans Canada (DFO), 2016. A Canadian Action Plan to Address the Threat of Aquatic Invasive Species. Canadian Council of Fisheries and Aquaculture Ministers Aquatic Invasive Species Task Group. http://www.dfo-mpo.gc.ca/science/environmental-environnement/ais-eae/ publications/plan/page01-eng.html. Early, R., Bradley, B.A., Dukes, J.S., Lawler, J.J., Olden, J.D., Blumenthal, D.M., Sorte, C.J., 2016. Global threats from invasive alien species in the twenty-first century and national response capacities. Nat. Commun. 7. Fanning, L., Mahon, R., McConney, P., 2011. Towards Marine Ecosystem-based Management in the Wider Caribbean. Amsterdam University Press, Amsterdam. Figueira, W.F., Booth, D.J., 2010. Increasing ocean temperatures allow tropical fishes to survive overwinter in temperate waters. Glob. Change Biol. 16 (2), 506e516.
mez Lozano, R., Anderson, L., Akins, J.L., Buddo, D.S.A., García-Moliner, G., Gourdin, F., et al., 2013. Regional Strategy for the Control of Invasive Lionfish in Go the Wider Caribbean, vol.31. International Coral Reef Initiative. ftp://ftp.fao.org/FI/DOCUMENT/wecafc/15thsess/ref10e.pdf. ^ te
, I.M., 2012. Invasive lionfish drive Atlantic coral reef fish declines. PLoS One 7 (3), e32596. Green, S.J., Akins, J.L., Maljkovi
c, A., Co Hackerott, S., Valdivia, A., Cox, C.E., Silbiger, N.J., Bruno, J.F., 2017. Invasive lionfish had no measurable effect on prey fish community structure across the Belizean Barrier Reef. PeerJ 5, e3270. Haddad, V., Stolf, H.O., Risk, J.Y., França, F.O., Cardoso, J.L.C., 2015. Report of 15 injuries caused by lionfish (pterois volitans) in aquarists in Brazil: a critical assessment of the severity of envenomations. J. Venom. Animals Toxins Incl. Trop. Dis. 21 (1), 1. Halpern, B.S., Diamond, J., Gaines, S., Gelcich, S., Gleason, M., Jennings, S., et al., 2012. Near-term priorities for the science, policy and practice of coastal and marine spatial planning (CMSP). Mar. Policy 36 (1), 198e205. Harvey, R.G., Mazzotti, F.J., 2014. The Invasion Curve: a Tool for Understanding Invasive Species Management in South Florida. IFAS Publication Number WEC347. University of Florida, Gainesville, FL. edis. ifas. ufl. edu/uw392. Hewitt, C.L., Everett, R.A., Parker, N., 2009. Examples of current international, regional, and national regulatory frameworks for preventing and managing marine bioinvasions. In: Rilov, G., Crooks, J.A. (Eds.), Biological Invasions in Marine Ecosystems Ecological, Management, and Geographic Perspectives. Springer-Verlag, Berlin, Heidelberg, pp. 335e349. Johnston, M.W., Purkis, S.J., 2015. Hurricanes accelerated the FloridaeBahamas lionfish invasion. Glob. Change Biol. 21 (6), 2249e2260. Kannan, V., 2015. Globalization and government regulations: invasive species management in an era of interdependence. J. Crit. Writ. 10, 8e12. €koski, E., Çinar, M.E., Oztürk, B., et al., 2014. Impacts of invasive alien marine species on ecosystem Katsanevakis, S., Wallentinus, I., Zenetos, A., Leppa services and biodiversity: a pan-European review. Aquat. Invasions 9 (4), 391e423. Kilgo, J.M., 2014. Lionfish Response Management Plan U.S. Virgin Islands. Update February 2014. http://lionfish.gcfi.org/sites/default/files/documents/ lionfishplan_usvi_update_feb2014_sm.pdf. (Accessed 6 December 2016). Kling, D.M., Sanchirico, J.N., 2014. Controlling Marine Invasive Species: the Case of the Indo-Pacific Lionfish Invasion in the Southeast US and Caribbean. California Sea Grant College Program, UC San Diego. http://escholarship.org/uc/item/7zz429tm#page-3. (Accessed 3 August 2017). Kulbicki, M., Beets, J., Chabanet, P., Cure, K., Darling, E., Floeter, S.R., et al., 2012. Distributions of Indo-Pacific lionfishes Pterois spp. in their native ranges: implications for the Atlantic invasion. Mar. Ecol. Prog. Ser. 446, 189e205.

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R.E. Graham, L.M. Fanning / Global Ecology and Conservation 12 (2017) 253e262

Layman, C.A., Allgeier, J.E., 2012. Characterizing trophic ecology of generalist consumers: a case study of the invasive lionfish in the Bahamas. Mar. Ecol. Prog. Ser. 448, 131e141. Lesser, M.P., Slattery, M., 2011. Phase shift to algal dominated communities at mesophotic depths associated with lionfish (Pterois Volitans) invasion on a bahamian coral reef. Biol. Invasions 13 (8), 1855e1868. Lopez, V., Krauss, U., 2006. National and Regional Capacities and Experiences on Marine Invasive Species, including Ballast Waters, Management Programmes in the Wider Caribbean Region-a Compilation of Current Information. CABI, Trinidad & Tobago. UNEP. Mahon, R., Fanning, L., McConney, P., 2014. Assessing and facilitating emerging regional ocean governance arrangements in the Wider Caribbean Region. Ocean. Yearb. 28, 631e671. ^ te
, I.M., 2016. Managing marine invasive species through public participation: lionfish derbies as a case study. Mar. Policy Malpica-Cruz, L., Chaves, L.C., Co 74, 158e164. Miloslavich, P., Díaz, J.M., Klein, E., Alvarado, J.J., Díaz, C., Gobin, J., et al., 2010. Marine biodiversity in the Caribbean: regional estimates and distribution patterns. PLoS One 5 (8), e11916. Mohammed, E., 2016. Implementation report (2013-2015): regional strategy for the control of the invasive lionfish in CRFM member states. No. 2016/02 CRFM Tech. Advis. Document 58. Morris Jr., J.A., 2012. Invasive Lionfish: a Guide to Control and Management. Series Number 1. Gulf and Caribbean Fisheries Institute Special Publication, Marathon, Florida, USA, p. 113. Morris Jr., J.A., Whitfield, P.E., 2009. Biology, Ecology, Control and Management of the Invasive Indo-Pacific Lionfish: an Updated Integrated Assessment. http://aquaticcommons.org/2847/1/NCCOS_TM_99.pdf. National Invasive Species Council, (NISC), 2001. Meeting the Invasive Species Challenge: National Invasive Species Management Plan, vol.80. https://www. doi.gov/sites/doi.gov/files/migrated/invasivespecies/upload/2001-Invasive-Species-National-Management-Plan.pdf. Peiffer, F., Bejarano, S., de Witte, G.P., Wild, C., 2017. Ongoing removals of invasive lionfish in Honduras and their effect on native Caribbean prey fishes. PeerJ 5, e3818. Perry, C.T., Murphy, G.N., Kench, P.S., Smithers, S.G., Edinger, E.N., Steneck, R.S., Mumby, P.J., 2013. Caribbean-wide decline in carbonate production threatens coral reef growth. Nat. Commun. 4, 1402. Premo, D., Clarke, C., Stine, A., Hindelang, M., 2014. Keweenaw bay indian community aquatic invasive species adaptive management plan. White Water Assoc. Inc. 1e44. http://nrd.kbic-nsn.gov/sites/default/files/KBIC%20Final%20AIS%20Plan%20Approved_Merged.pdf. Rocha, L.A., Rocha, C.R., Baldwin, C.C., Weigt, L.A., McField, M., 2015. Invasive lionfish preying on critically endangered reef fish. Coral Reefs 34 (3), 803e806. Schofield, P.J., 2010. Update on geographic spread of invasive lionfishes (Pterois volitans [linnaeus, 1758] and P. Miles [bennett, 1828]) in the western north Atlantic Ocean, caribbean sea and Gulf of Mexico. Aquat. Invasions 5 (Suppl. 1), S117eS122. Simberloff, D., 2005. Non-native species do threaten the natural environment! J. Agric. Environ. Ethics 18 (6), 595e607. Simmons, K.R., 2014. Evidence of the Enemy Release Hypothesis: Parasites of the Lionfish Complex (Pterios Volitans and P. Miles) in the Western North Atlantic, Gulf of Mexico, and Caribbean Sea. http://nsuworks.nova.edu/cgi/viewcontent.cgi?article¼1009&context¼occ_stuetd. Tahoe Regional Planning Agency (TRPA), 2014. Lake Tahoe Region Aquatic Invasive Species Management Plan, California - Nevada, vol.35. https://www.fs. usda.gov/Internet/FSE_DOCUMENTS/stelprd3812963.pdf. U.S. Environmental Protection Agency (EPA), 2008. Effects of climate change for aquatic invasive species and implications for management and research. National Center for Environmental Assessment, Washington, DC; EPA/600/R-08/014. Available from the National Technical Information Service, Springfield, VA, and online at http://www.epa.gov/ncea. Walters, L.M., Jones, K.G., 2012. Caribbean Food Import Demand: Influence of the Changing Dynamics of the Caribbean Economy. Presentation at the Southern Agricultural Economics Association Annual Meetings. February 4-7. Birmingham, AL. http://ageconsearch.umn.edu/bitstream/119724/2/ 119724.pdf. Waugh, J.D., 2009. Neighborhood Watch: Early Detection and Rapid Response to Biological Invasion along US Trade Pathways. IUCN. http://www. indiaenvironmentportal.org.in/files/nw_webfinal.pdf.