Original ArticleThe value of monitoring in efficiently and adaptively managing biotoxin contamination in marine fisheries
Introduction
Harmful algal blooms (HABs) represent an increasingly significant threat to fisheries and aquaculture globally. In some, but not all, regions (Hallegraeff et al., 2021), they are increasing in size, frequency, and duration due in part to the combined effects of eutrophication and climate change (Glibert, 2020; Hallegraeff, 2010, 1993; Van Dolah, 2000) and these trends are expected to persist or worsen with continued climate change (“high confidence” in (IPCC, 2019)). Many HABs are harmful because they produce toxins that accumulate in species harvested by fisheries and aquaculture and can cause human illness or mortality when consumed in high doses (Grattan et al., 2016). As a result, toxin levels in vulnerable seafood species are closely monitored and elevated levels often trigger the closure of fisheries and aquaculture operations, which can undermine their economic, nutritional, and sociocultural value (Bauer et al., 2010; Ritzman et al., 2018; Trainer et al., 2020a). Designing biotoxin monitoring and management programs that effectively protect public health with minimal impacts to fishing and aquaculture operations is critical to maintaining the viability of coastal communities in a changing ocean.
On the North American West Coast, diatoms in the Pseudo-nitzschia genus can produce the neurotoxin domoic acid, which can cause amnesic shellfish poisoning (ASP) when shellfish containing elevated levels of the toxin are consumed by humans. The symptoms of ASP range from gastrointestinal issues (e.g., stomach pain, vomiting, diarrhea, etc.) to neurological issues (e.g., headaches, dizziness, confusion, memory loss, seizures, etc.) to, in rare cases, death (Teitelbaum et al., 1990). The first cases of ASP and its linkage to Pseudo-nitzschia and domoic acid were documented in eastern Canada in 1987 (Bates et al., 1989; Perl et al., 1990; Wright et al., 1989) and domoic acid contamination has been monitored in several commercially and recreationally harvested seafood species on the U.S. West Coast since 1991 (CA-OST, 2016a). Domoic acid commonly enters the food web through filter feeders such as mussels, clams, and anchovies and is then transferred to predators such as crabs, lobsters, and fish (Lefebvre et al., 2002). Bivalves and crustaceans generally exhibit the highest risk of contamination, are monitored the most frequently, and receive the greatest regulatory oversight in their fisheries and farming operations.
HABs of Pseudo-nitzschia are significantly increasing in the U.S. (Hallegraeff et al., 2021). In 2015, a marine heatwave known as “the blob” caused a Pseudo-nitzschia bloom of unprecedented size and duration (McCabe et al., 2016; McKibben et al., 2017). The bloom spanned from southern California to Alaska (McCabe et al., 2016) and resulted in expansive and prolonged closures of commercial and recreational fisheries (Ekstrom et al., 2020). The Dungeness crab fishery, among the most lucrative fisheries on the U.S. West Coast (hereafter West Coast), was hit especially hard (Fisher et al., 2021; McCabe et al., 2016; Moore et al., 2019). The California season was delayed by 6 months in some regions and was declared a federal fisheries disaster with over $25 million in relief aid distributed to impacted fishers, dealers, and processors (Bonham, 2018; Holland and Leonard, 2020). In addition to financial losses, the individuals living and working in West Coast fishing communities reported losses to emotional well-being and sense of place (S. K. Moore et al., 2020; Ritzman et al., 2018). Many individuals expressed mistrust in the handling of the closures surrounding the event and skepticism about the severity of the health risk (Ekstrom et al., 2020). Ekstrom et al. (2020) and Ritzman et al. (2018) suggest that this mistrust stemmed from the appearance of arbitrary and inconsistent management across states. For example, the commercial Dungeness crab fishery in northern California remained closed months after southern Oregon had opened, leading fishers to believe that agencies were using political boundaries rather than physical ones to implement closures (Ritzman et al., 2018). In addition, the commercial Dungeness crab fishery was closed in some parts of California while the recreational fishery remained open with an advisory to remove contaminated viscera, leading to confusion around the public health risk of domoic acid (Ekstrom et al., 2020). This highlights a dual need to demonstrate the credibility of the science supporting toxin monitoring and management and to standardize best practices across fisheries and management boundaries.
The monitoring and management of domoic acid in the West Coast Dungeness crab fishery (Fig. 1; Tables S1, S2) is based on design principles common to most biotoxin monitoring and management programs (Langlois and Morton, 2018; Park et al., 1999). First, a level of contamination that triggers management action is specified. The action level for Dungeness crab is 20 ppm domoic acid in the meat or 30 ppm in the viscera (guts) based on the analysis of data from the 1987 ASP outbreak (Toyofuku, 2006; US-FDA, 2019; Wekell et al., 2004). Second, criteria for determining when to take or cease management actions based on this action level is defined. In all three West Coast states, a fishing area will open if each of six crabs collected from the area test below the action level. If one or more of the collected crabs test above the action level, management action is taken and is only ceased when two successive surveys, conducted at least 7 days apart, test clean (each of six crabs below the action level). Third, the spatial-temporal frequency of monitoring and size and arrangement of the associated management zones is determined. Decisions related to this third principle are arguably the most critical to determining the ability of management to efficiently respond to changes in toxin contamination and all three states have employed different approaches to this critical dimension of biotoxin monitoring. Finally, management actions for responding to high levels of toxin contamination are identified. When the 2015 HAB event hit, the only management action available to West Coast states was to employ area closures.
After the surprise of the 2015 HAB event and its devastating impact on coastal communities, all three states made modifications to their biotoxin monitoring and management plans (Fig. 1). In Nov 2017, Oregon passed legislation to allow the use of “evisceration orders” as an alternative to full fishery closures (ODA, 2017). Evisceration orders require the removal of crab viscera, which harbor the greatest domoic acid contamination (Wekell et al., 1994), in the event that the viscera tests above the action level but the meat tests below the action level. Although eviscerated crabs often receive lower market prices (Hackett et al., 2003), this option presents the fishing industry with some flexibility during extended closures. Oregon also more than doubled its number of biotoxin monitoring sites for Dungeness crab, presumably increasing the efficiency with which management can react to changes in contamination, and delineated clear management boundaries, facilitating rapid and objective decision-making for managers and increasing predictability for fishers (ODA, 2017). In Oct 2020, California delineated domoic acid management boundaries and adopted rules to require sampling at sites that were previously sampled voluntarily, though consistently (CDFW, 2020a). In Oct 2021, it legalized evisceration orders as a management option (McGuire, 2021). In Feb 2021, Washington adopted an emergency rule temporarily allowing evisceration orders (WDFW, 2021) and is currently considering legislation to grant long-term authority for issuing evisceration orders and to fund expanded testing of crab harvested in the Puget Sound (Chapman and Pollet, 2021). Although intuitively beneficial, these expansions come with increased costs. Understanding the benefits of these expansions is therefore necessary to justify increased spending on biotoxin monitoring and to increase stakeholder trust in the effectiveness of these measures.
Simulation testing and power analysis are powerful tools for quantitatively measuring the ability of monitoring programs to track ecosystem dynamics and to accurately and effectively inform management (Field et al., 2007; Legg and Nagy, 2006). Simulation testing leverages ‘operating models’ that attempt to replicate the dynamics of a system as a platform for comparing alternative monitoring and management programs with predefined performance metrics. Power analyses are a class of simulation methods used to determine the minimum sample size required to detect an effect of a given size, or the corollary, the minimum size of an effect that can be determined by a given sample size. Simulation testing and power analysis are commonly used to evaluate the performance of wildlife monitoring surveys for fish (Parker et al., 2016), birds (Thomas, 1996), mammals (Kendall et al., 1992), reptiles (Sewell et al., 2012), and amphibians (Barata et al., 2017), but only a few studies have used these approaches to evaluate biotoxin monitoring programs. For example, (Solow et al., 2014) used power analysis to optimize the number and arrangement of monitoring sites for resting cysts of the harmful alga Alexandrium catenella in the Gulf of Maine, and (Fontana et al., 2020) applied a similar approach for biotoxin contamination in bivalve aquaculture in Brazil. Wider utilization of tailored simulation testing in the design of biotoxin monitoring programs – whether for benthic resting cysts, pelagic algal blooms, or contamination in wild, farmed, or sentinel (i.e., placed by humans for monitoring) species – could assist in establishing scientific foundations for defining program attributes (e.g., sample sizes, site arrangement, etc.) and finding cost-effective solutions that protect public health while limiting impacts on fishers. In turn, this could serve to justify the costs of monitoring and build stakeholder trust.
This study used a two-pronged approach to evaluate the value of biotoxin monitoring in facilitating efficient and adaptive management that protects public health with the least impact on fishing communities. First, a review of historical domoic acid monitoring and management programs in the West Coast Dungeness crab fishery is used to identify design principles that have promoted efficient and adaptive management. Second, a simulation model and power analysis based on this system is used to quantitatively measure the benefits of expanded monitoring for jointly achieving public health and fisheries objectives. Although focused on the West Coast Dungeness crab fishery and domoic acid contamination, this study reveals principles relevant to the design of monitoring and management programs for other regions, species, and biotoxins. It also highlights the powerful but underutilized role of simulation testing and power analysis in anticipating and comparing the performance of alternative biotoxin monitoring programs and management strategies.
Section snippets
Monitoring history
Domoic acid testing results from state-run biotoxin monitoring programs were provided by the California Department of Public Health (CDPH), Oregon Department of Agriculture (ODA), and Washington Department of Health (WDOH). The records were variable in temporal coverage but all spanned 2015 to 2021 (Fig. 2B). The test results primarily described domoic acid contamination in Dungeness crab (Metacarcinus magister), razor clam (Siliqua patula), and California mussel (Mytilus californianus) but
Washington
Of the three states, Washington experienced the lowest domoic acid contamination and least expansive closures during the 2015-16 commercial Dungeness crab fishing season because of the 2015 HAB event (Fig. 2AB). However, Washington was the only state to conduct mid-season sampling during the 2014-15 season (May 2015), initiated in response to elevated domoic acid levels in razor clam samples (Fig. 2C) (Wilson, 2018), and ultimately closed its fishery for much of the remaining season. Washington
Discussion
After the massive 2015 HAB and subsequent closures of the lucrative commercial Dungeness crab fishery, West Coast states increased the efficiency of Dungeness crab domoic acid monitoring and management by: (1) expanding the spatial-temporal frequency of monitoring; (2) delineating clear management zones; and (3) legalizing evisceration orders as a potential mitigation option. These actions have already served to protect public health while limiting impacts on fishing communities. In Oregon,
Conclusion
This study provides a synthetic portrait of biotoxin monitoring and management in the U.S. West Coast's most lucrative commercial fishery and illustrates how states have changed their monitoring and management programs in response to mounting HAB risk. This provides an instructive template for other regions threatened by increasing risk of contamination in marine seafood. Specifically, it highlights the value of (1) designing the spatial-temporal frequency of monitoring to reflect the
Declaration of Competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We are grateful to Tracie Barry (WDOH), Alex Manderson (ODA), Christina Grant (CDPH), Duy Truong (CDPH), Vanessa Zubkousky (CDPH), and Matthew Hunter (ODFW) for providing data from state-run biotoxin monitoring programs and to the many other scientists, fishermen, and farmers involved in collecting and processing this data. We thank ORHAB and its member partners for providing Pseudo-nitzschia abundance and particulate domoic acid data along the Washington coast. The Olympic Region Harmful Algal
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