Discussion
In this study, a MCDA risk ranking framework integrating empirical data and expert opinion was used to rank pathogens in the live baitfish pathway. Applying the framework as a case study to the problem of pathogen introduction via the Minnesota bait pathway resulted in distinct risk scores for each of the 15 pathogens assessed. The highest-risk pathogen group included the Asian fish tapeworm, O. ovariae, VHSV, FHMNV, IPNV, A. salmonicida and Y. ruckeri . To our knowledge, this is the first study that has employed both semi-quantitative scores and expert opinions to evaluate and rank pathogens in the live baitfish pathway. The inclusion of expert judgement in the risk ranking exercise allowed a more detailed ranking analysis with distinct risk scores, avoiding the risk score clustering observed in the unweighted system. The weighted framework also made explicit the impact of subjective beliefs about which criteria were most important, emphasizing the importance of considering value judgements when making decisions about which pathogens to manage.
The Asian fish tapeworm, O. ovariae, and VHSV were the top-ranked pathogens in both the unweighted and weighted risk scoring systems, confirming the relevance of these three fish pathogens to the bait supply pathway. The highest ranked pathogen was the non-native Asian fish tapeworm, a generalist fish parasite that can infect hundreds of fish species and known to be present in the live baitfish supply in the region (Boonthai et al. 2017; Kuchta et al. 2018). Ovipleistophora ovariae is an obligate intracellular and vertically transmitted parasite, infecting the ovarian tissue of golden shiners, leading to significant declines in fecundity by age-2 (Phelps & Goodwin, 2008). Although O. ovariae is believed to be widely distributed and highly prevalent in the golden shiner supply chain, surveys of wild populations to confirm establishment have not been completed (McEachran et al. in review), and the parasite remains of concern. Indeed, a previous qualitative risk assessment for golden shiners imported from Arkansas bait producers identified both Asian fish tapeworm and O. ovariae as high-risk (J. L. Gunderson, 2018)(J. Gunderson, 2004).VHSV is a broadly recognized risk to fish health globally (Escobar, Escobar-Dodero, & Phelps, 2018), and following its invasion in the Great Lakes in 2003 (Elsayed et al., 2006), has been identified as a concern in previous evaluations of the Minnesota bait industry (Boersen et al., 2017; Phelps, Craft, Travis, Pelican, & Goyal, 2014).
The results of the risk ranking framework highlight the paradoxes of risk management efforts that focus on the host species, rather than the pathogen of interest. For example, the ranking framework identified the Minnesota certifiable diseases IPNV, A. salmonicida , and Y. ruckeri as high-risk hazards for the bait pathway. These pathogens can have serious fish health implications for salmonid species (Furones, Rodgers, & Munn, 1993; Roberts & Pearson, 2005; Wiklund & Dalsgaard, 1998) and are consequently regulated in Minnesota to limit introduction and spread (MN Statute 17.4982). However, these regulations only apply to salmonid species, despite known susceptibility and evidence of at least A. salmonicida and Y. ruckeri in the local retail baitfish supply (McEachran et al, in review). In contrast, VHSV is another state-certifiable pathogen identified as high-risk in this study, but it is managed at the pathogen level, with all susceptible species (including legal bait species) subject to regulatory conditions (MN Statute 17.4991). These paradoxes highlight the importance of managing specific invasive pathogens of known risk, rather than host species, when attempting to reduce the risk of pathogen spread via any live animal movement pathway.
Estimates of evidence uncertainty varied across pathogens, with some pathogens having higher or lower uncertainty than average (Figure 3a). Some pathogens in the high-risk group (e.g. FHMNV and IPNV) and low-risk pathogens (e.g. WSBV, FHMPV) obtained high uncertainty scores, suggesting that as more information becomes available in the future, the risk ranking may change for these less well-described pathogens. Because of the high number of fish species and increasing rates of pathogen reporting and surveillance, pathogens of fish account for a large number of emerging diseases of wildlife (Tompkins et al., 2015), and so invasion management tools must be equipped to dealing with both emergent and well-documented pathogens. Fish health managers could apply the risk ranking to evaluate potential risk and determine what type of action, if any, is warranted, based on their own tolerance for uncertainty and risk (Figure 3b). If new evidence emerges in the future, the risk ranking framework can be updated and risk ranking scores recalculated, providing support for risk-based disease management.
It is important to note that while the risk ranking framework identifies pathogens of importance (‘high risk’) in the live baitfish supply, this does not directly translate to an inevitable impact on wild fish populations. Like all invasion scenarios, many factors must align to result in the successful establishment and negative outcome of a hazard (e.g. baitfish pathogen) to a new environment (e.g. naïve wild population of concern) (Simberloff, 2009; Stohlgren & Schnase, 2006; Wang & Jackson, 2011). Examples of failed introductions are impossible to quantify given the limited information for the disease status of baitfish and their movement patterns, and the disease status of wild populations. For VHSV, a pathogen where significant surveillance has occurred (i.e. Phelps et al. 2014), no detections have occurred in the Minnesota baitfish supply and therefore transmission via this pathway is presumed to be nonexistent. Evaluating the current distribution and potential for establishment of high-risk pathogens known to be in the baitfish supply (e.g. O. ovariae , A. salmonicida , Y. ruckeri ) is warranted to better inform future risk assessments. Regardless, the risk ranking framework is a useful tool to identify and prioritize pathogens for further management consideration and provide justification for proactive prevention efforts.
Incorporating variability and uncertainty from multiple different stakeholder groups (managers, academia, and industry), and not just a single sector, is increasingly recognized as a critical part of managing invasive species (Shackleton et al., 2019). The expert opinion-based risk ranking framework developed in this study incorporates expert opinion with empirical evidence, and improves on previous qualitative evaluations and unweighted rankings to distinguish between high-, medium-, and low-risk pathogens in the live baitfish supply. Where uncertainty exists, the precautionary principle is often employed, whereby novel and highly uncertain pathogens are automatically assigned a high-priority ranking and allocated resources and risk management efforts (Larson et al., 2013; Sainsbury & Vaughan-Higgins, 2012) This approach risks obfuscating management plans and creating burdensome regulations for producers (van Senten & Engle, 2017). Conversely, failure to systematically assess all possible hazards may indeed overlook important pathogens, leaving fish populations at risk (Gaughan, 2001). Although the framework discussed in this study provides a relative, rather than an absolute determination of risk, disease management in the absence of a structured and inclusive process for identifying hazards could result in the over or under-inclusion of important pathogens. This framework has broad applicability for understanding risks and will provide support for difficult conservation decisions to balance invasion risks with the economic, cultural, and societal benefits associated with live baitfish use. In addition, its flexibility in application means it could be modified to assess risks in other pathways, jurisdictions, or other taxa of invasive species as invasion prevention needs emerge.