Threat assessment for Pacific sand lance (Ammodytes personatus) in the Salish Sea

Abstract

Like many forage fish species, Pacific sand lance (Ammodytes personatus) play a key role in nearshore marine ecosystems as an important prey source for a diverse array of predators in the northeastern Pacific. However, the primary threats to Pacific sand lance and their habitat are poorly defined due to a lack of systematic data. Crucial information needed to assess their population status is also lacking including basic knowledge of their local and regional abundance and distribution. Sand lance are currently listed as ‘not evaluated’ under the IUCN red list and they have not been assessed by US and Canadian agencies. This hampers management and policy efforts focused on their conservation. To address this knowledge gap, we conducted a three-part, structured expert elicitation to assess the vulnerability of Salish Sea sand lance populations. Experts were asked to list and rank key threats to Salish Sea sand lance and/or their habitat, to further quantify the vulnerability of sand lance to identified threats using a vulnerability matrix, and to predict the population trajectory in 25 years from today. Impacts associated with climate change (e.g. sea level rise, sea temperature rise, ocean acidification, and extreme weather) consistently ranked high as threats of concern in the ranking exercise and quantified vulnerability scores. Nearly every expert predicted the population will have declined from current levels in 25 years. These results suggest sand lance face numerous threats and may be in decline under current conditions. This research provides vital information about which threats pose the greatest risk to the long-term health of sand lance populations and their habitat. Managers can use this information to prioritize which threats to address. Future research to reliably quantify population size, better understand the roles of natural and anthropogenic impacts, and to identify the most cost-effective actions to mitigate multiple threats, is recommended.

Introduction

Pacific sand lance, Ammodytes personatus (hereafter, sand lance), are small forage fish that play a significant role in the nearshore ecosystem of the northeast Pacific Ocean. Sand lance are known to comprise part of the diet for at least 100 predators (Robards and Piatt, 1999; Penttila, 2007; Harvey et al., 2010; Alheit and Peck, 2019; Staudinger, 2020; Scordino et al., 2022; Shaffer et al., 2023). Examples include seabirds, especially Alcids (Robards and Piatt, 1999; Zamon, 2000; Pastran et al., 2021); fish such as Chinook (Oncorhynchus tshawytscha) and coho salmon (Oncorhynchus kisutch; Duguid, 2020), Pacific cod (Gadus macrocephalus;Gunther et al., 2023), and lingcod (Ophiodon elongatus; Beaudreau and Essington, 2007); and larger mammals like Steller sea lions (Eumetopias jubatus; McKenzie and Wynne, 2008), harbor seals (Phoca vitulina richardii; Lance et al., 2012), and baleen whales such as humpback (Megaptera novaeangliae; Wright et al., 2016), minke (Balaenoptera acutorostrata; Okamura et al., 2009; Towers et al., 2019) and fin (Balaenoptera physalus; Moore et al., 2019). They play a particularly important role during the breeding of seabirds because of the high energy content, and slender bodies that are easily transported to, and consumed by, chicks (Willson et al., 1999; Bertram et al., 2001; Hedd et al., 2006; Beaubier and Hipfner, 2013). Sand lance range from California to Alaska and are one species within the Ammodytes genus, the only species that occurs in the Salish Sea, and one of two in the eastern Pacific (Robards and Piatt, 1999; Orr et al., 2015). They are dependant on specific spawning and burying habitats that must have coarse, silt-free, well oxygenated sandy substrates (hereafter “habitat”) (Baker et al., 2024). Declines in sand lance abundance could have serious rippling impacts on coastal ecosystems given their important role in the food web (Bertram et al., 2001; Robards et al., 2002; Piatt et al., 2020).

Piecemeal observations by researchers, including some of the authors, Indigenous groups, and anecdotal reports from recreational anglers in the northeastern Pacific over the last decade have resulted in a growing concern that forage fish, including sand lance populations, face numerous threats (Dethier et al., 2016; Frick et al., 2022; Robinson et al., 2023). While some research has been undertaken on their biology (Penttila, 2007; Haynes et al., 2008; Haynes and Robinson, 2011; Hipfner and Galbraith, 2013; Matta and Baker, 2020; Zhukova and Baker, 2022; Robinson et al., 2023), distribution and seasonal abundance (Selleck et al., 2015), and habitat distribution (Robinson, 2013; Baker et al., 2019; Robinson et al., 2021; Huard et al., 2022; Baker et al., 2023; Gunther et al., 2023), there is a lack of comprehensive empirically derived information to contextualize their population status at a scale as wide as the Salish Sea.

Sand lance have an uneven distribution throughout their range, often restricted to small, specific, and patchy habitats that are not well mapped (Haynes et al., 2008; Robinson et al., 2013; Speed and Baker, 2016; Greene et al., 2020; Robinson et al., 2021; Huard et al., 2022). Their occurrence is temporally variable (Selleck et al., 2015) and they are dormant much of the winter (van Deurs et al., 2010; Haynes and Robinson, 2011; Robinson et al., 2013; Greene et al., 2015; Baker et al., 2019, 2023). Accurate estimates employed in the North Sea require use of both acoustics and nets at great cost with imperfect results (Greenstreet et al., 2006, 2010). There has been limited species-specific population assessments at the Salish Sea scale, and one projecting forward in the US side of the Salish Sea. In Washington State, field surveys targeting the San Juan Channel sand wavefield (approximately 0.6 km²) have occurred over the past 15 years estimating that there is an average of 81 million sand lance (Blaine, 2006; Baker et al., 2019; Baker et al., 2024); however, these surveys are limited to one area and do not speculate on population trends (Speed and Baker, 2016; Greene et al., 2020, Greene et al., 2021). The National Oceanic and Atmospheric Administration (NOAA) has conducted research on abundance trend estimates for several forage fish within Puget Sound and found sand lance populations increased in some basins over the study time (1971-1985; 2002-2003) (Greene et al., 2015). A handful of additional studies relating to Pacific sand lance in the Salish Sea exist, however they lack specific temporal, spatial, or species-specific assessments to be useful to understanding the sand lance population trends (Penttila, 1995; Selleck et al., 2015) (Tomlin et al., 2021) (Bertram and Kaiser, 1993; Hedd et al., 2006; Thayer et al., 2008) (Gunther et al., 2023), (Duguid, 2020; Baker et al., 2021) (Einoder, 2009). The historical lack of research conducted on sand lance may have contributed to the lack of knowledge and research into population status as it can be difficult to acquire research funding if there is no/little demonstratable risk to the species or ecosystem.

There are multiple, potentially interacting threats on sand lance in the Salish Sea (Krueger et al., 2010; Hipfner et al., 2018; Baker et al., 2019; Buchanan et al., 2019; Liedtke and Conn, 2021; Selden and Baker, 2023). The Salish Sea is a densely populated area on the Northeastern Pacific coast where rapid anthropogenic growth and development is exerting increasing pressure on regional biodiversity (Gaydos and Pearson, 2011; Gaydos et al., 2015; Singh et al., 2017). Anthropogenic activities in the Salish Sea have the potential to negatively impact sand lance populations and habitat, which could result in cascading effects (Staudinger, 2020). As a species with an obligate association to very specific, rare habitats, sand lance are particularly exposed to impacts from habitat loss and degradation (Pearson et al., 1984; Quinn, 1999; Robinson et al., 2013; Bizzarro et al., 2016; Huard et al., 2022; Smith and Liedtke, 2022).

While many threats have been documented individually, including the vulnerability of sand lance to climate change (Hare et al., 2016; Rovellini et al., 2024), there is no comprehensive list of threats acting on sand lance. These data deficiencies make it challenging to understand pressures on sand lance, and to prioritize management actions to abate threats. Evaluating the key threats would help to understand drivers of decline and inform decisions to conserve and manage sand lance.

In this study, we sought to overcome these challenges through the use of expert judgement to identify a comprehensive list of threats to their persistence, including a ranking of the vulnerability of sand lance to those threats, and to develop a hypothesis for Salish Sea sand lance population trends. Structured expert elicitation is routinely applied in conservation and decision-making contexts, when data are incomplete or unavailable, and time and resources to collect such data are limited (Wolfson et al., 1996; Harwood, 2000; Wilson et al., 2005; De Lange et al., 2010; Martin et al., 2012; Burgman et al., 2015; The Salish Sea Pacific Herring Assessment and Management Strategy Team, 2018). Structured approaches are designed to facilitate the elicitation of expert judgement in such a way that common biases are mitigated, and the resulting data conform to the same level of empirical control and transparency afforded to other forms of empirical data and have been shown to improve the accuracy and calibration of results (Hemming et al., 2018; Camaclang et al., 2021; Hanea et al., 2022).

Ranking the potential impact of threats requires a clear definition of each and connecting such impacts with putative individual or population-level effects across a range of exposure levels (O’Hagan, 2019). Direct ranking methods are often expedient, but can over-rely on the opinions of experts, and may result in availability biases, with threats that are more easily recalled, or more familiar to experts, being listed higher than other threats (e.g., Donlan et al., 2010). Indirect methods, by contrast, identify explicit criteria for assessing the magnitude of any threat, and can be more time consuming, but may guard against availability bias. In ecology, vulnerability is often categorized into exposure, sensitivity, and resilience. However; there are a number of different approaches (Van Straalen, 1993; Turner et al., 2003; Wilson et al., 2005; De Lange et al., 2010; Speirs-Bridge et al., 2010; Beroya-Eitner, 2016; Berrouet et al., 2018; Hou et al., 2022) requiring a choice to be made about the best criteria to represent vulnerability for the species and ecosystems in question. We used both indirect and direct ranking methods to help order the list of threats, choosing to adapt the methods and vulnerability scores developed by Halpern et al. (2007) and Teck et al. (2010); and repeated by Grech et al. (2011) and Kappel et al. (2012) as applied in the marine realm to the top ranked threats of concern. The focus of our study was to expand the knowledge of sand lance and their habitats to support ecosystem conservation. Specifically, we aimed to:

• Create a list of threats to sand lance habitats and populations;

• Rank the threats through a vulnerability assessment to identify those with the highest potential to reduce populations and/or their critically required habitat; and

• Generate a hypothesis on the population trajectory of sand lance.

Methods

We applied the IDEA protocol for structured expert elicitation (Investigate, Discuss, Estimate, and Aggregate); (Hanea et al., 2018; Hemming et al., 2018). We began our assessment of threats to sand lance with a literature review to identify a list of threats. We then supplemented this list through an expert elicitation. This aimed to overcome biases in the literature due to publication biases, such as demographic biases, as well as lags in the literature whereby emerging threats may not have been documented or sufficiently studied for publication (Baum and Martin, 2018).

This research was undertaken under the University of British Columbia Human Ethics H19-01635 for the Salish Sea Cumulative Threats project, led by Dr. Tara Martin. The expert elicitation took place from January – April 2021, using remote elicitation. To address our questions, we administered three sequential surveys (Surveys were delivered through Qualtrics [https://www.qualtrics.com/]), through following the workflow of:

• Recruitment of experts.

• Survey 1: Initial review of threats and definitions.

• Videoconference: Provide feedback on Survey 1 and introduce process for Surveys 2 and 3.

• Survey 2: Initial estimate of population size and vulnerability assessment of threats.

• Survey 3: Review of Survey 2 results and finalize estimates.

Recruitment of experts

Species and/or habitat experts were identified based on literature searches (including grey literature), word-of-mouth, and personal experience of the authors. A snowball technique was also used where invited participants were asked to forward the participation request to other potential knowledge holders. Anyone who self-identified as being knowledgeable on sand lance or on habitats in the Salish Sea was invited to participate. Over 80 invitations were extended, invitations (via e-mail) can be found in the Supplementary Material.

Participants were from federal government agencies (28.5%, 11), not-for-profit organizations or non-governmental organizations (23%, 7), academic institutions (20.5%, 2), consulting firms (7.8%, 1), First Nation governments (staff not necessarily Indigenous identifying individuals) (2.6%, 1), First Nation non-governmental organizations (staff not necessarily Indigenous identifying individuals) (2.6%, 1), and Other (5.1%, 2). Respondents identified as men (39.5%, 15), women (44.7%, 17), and prefer not to answer (15.8%, 7). Participants ranged in age from 25 to 75 years old, with a majority falling into the 25 to 34, and 35 to 44 years old bands. Four participants [10.3%] chose not to respond to the age demographic question. Respondents identified as White (70.5%), Hispanic or Latino (2.6%), and prefer not to answer (26.9%). When asked about their type of expertise, 71.8% of respondents identified having knowledge of sand lance; 10% identified having knowledge of habitats; 5.4% selected both of the previous two categories; and 12.8% identified having related but other knowledge (such as knowledge of forage fishes in general in the Salish Sea, and/or knowledge of species that rely on sand lance). When asked about geographical area of expertise, 64.1% identified as being most familiar with the Canadian Salish Sea (i.e., British Columbia), 25.6% identified as being most familiar with the American Salish Sea (i.e., Washington State), 7.7% identified as being familiar with the entire Salish Sea, and 2.6% identified as not having familiarity with the Salish Sea but feeling they were able to provide insight to threats regardless of location.

Survey 1 – threat identification

An initial list of 20 potential threats to sand lance and/or their habitats was developed from a literature review (see Supplementary Table S1 for initial threat list). Each threat was accompanied by a definition of the threat. This list was reviewed by a small group of five experts to further reduce linguistic ambiguity and compiled into Survey 1 for review by 39 experts. In Survey 1 experts were first asked to review the initial list of threats and, if desired, provide and describe up to five additional threats. They were then asked to categorize the threats into one of three broad tiers of impact to sand lance: Of Concern, Least Concern, and Uncertain. Within each of the three tiers, experts were asked to directly rank threats in order of greatest to least risk, with no ties permitted, to the persistence of sand lance and/or to the persistence of their habitats in the Salish Sea. This was used to help generate a Cumulative Rank Score (CRS) across experts and threats (See Supplementary Material for calculation methods).

A 1-hour video conference was held on January 23, 2022. During the video conference, participants were formally introduced to the project and reviewed and discussed the 20 threats of concern. They were then informed of the process for completing Surveys 2 and 3 and invited to raise any questions or concerns. Following the video call, the list of threats to include in Survey 2 was reorganized, reworded, and in some cases expanded or collapsed based on the discussions.

Survey 2: vulnerability assessment and expert population trajectory assessment

Survey 2 was split into two parts: i) an assessment of the population trajectory; and ii) the relative quantification of vulnerability scores for the top threats.

Vulnerability assessment

For the vulnerability assessment (Survey 2), we sought to reduce the number of threats provided from Survey 1 to avoid expert fatigue. To determine the list of threats to be assessed, we ranked the 42 threats that received at least one vote as being a threat Of Concern by the CRS score (See Supplementary Table S3). Following the survey, the top 20 threats categorized as being Of Concern were utilized (see Supplementary Material for specific methods used Supplementary Table S2). The final 20 threats under evaluation were divided into two groups (A and B) each with 10 threats. Participants were then assigned to either group based on the threats they indicated had the most familiarity with as indicated in Survey 1. Group A had 22 participants assigned to it and Group B had 21. A copy of Survey 2 can be found in the Supplementary Material S2.

Experts were also asked to characterize the level of certainty for their responses to a given threat and allowed space to provide caveats and qualifiers to contextualize their responses. The specific questions asked in the survey are shown in Table 1.

As per Halpern et al. (2007) and Teck et al. (2010), experts were asked to consider the vulnerability criteria for each threat on an annual basis, and assign a relative value (0-4 or 0-6) using a predefined drop-down list (Table 2). Data from expert responses were used to develop a weighted average vulnerability score to represent a relative measure of how vulnerable sand lance and their habitats are to each threat. This approach to calculating relative vulnerability of sand lance is mathematically represented as

where S_i,k is the value of threat i and a vulnerability measure k, and W is the weight assigned to vulnerability measure k, such that W_k≥0, ∑_k=1,…,4W_k=1. The weights are normalized so that they sum to one and were empirically derived using a multicriteria decision model. Resistance was estimated to explain 66.5% of the vulnerability (Teck et al., 2010), when experts were assessing the vulnerability of various scenarios with pre-determined values and, therefore, we used 0.665 for the weighting of resistance. For the weighting of the three scale-related criteria, we assumed that frequency, area, and duration were of equal weights and used 1 – 0.665 = 0.334 divided by 3 to give each a weight of 0.112.

Frequency, area, and duration vulnerability measure results were standardized to have the same 0 to 4 scale (by multiplying the vulnerability value by 4/6) so they are comparable and were all given equal weight to resistance. Then, for each expert’s vulnerability score, the values were divided by the highest possible score (4) to give a value between 0 and 1. Values closer to 1 represent higher estimated vulnerability to that threat and values closer to 0, lower vulnerability. For each threat, the mean and confidence intervals across the experts were calculated to provide a single weighted vulnerability score. The mean and confidence intervals were calculated using the DescTools package in R, ‘meanCI’ function using bootstrapping methods. The confidence intervals are the 2.5^th and 97.5^th centiles, or a 95% confidence interval of an equi-tailed, two-sided, nonparametric interval using a basic bootstrap interval.

Population trajectory assessment

There were concerns that quantifying the trajectory of sand lance may be too onerous for the experts to accurately assess given the species’ cryptic nature, boom-and-bust episodic reproductive cycles, and the lack of a stock assessment. To overcome these issues, the team elicited population trajectory predictions using questions of increasing resolution. Experts were asked to consider a hypothetical survey program that had averaged 100 fish per survey each year over the previous five years. Experts were then asked to consider if the same population in the Salish Sea was evaluated 25 years from present (year 2047) would there be an increase, decrease, or no change relative to the current five-year average. The timeframe of 25 years was used because it encompasses multiple generations of the sand lance life cycle and is within the realm of experience that can be reasonably predicted by expert participants. This question was accompanied by a visual image of potential changes in sand lance (Figure 1). The purpose of this framing was to convey population changes of sand lance in a hypothetically observable and meaningful quantity for experts (a key criterion for structured expert elicitation questions [Hemming et al., 2018]).

Figure 1

Finally, experts were asked to quantify their estimates by providing their: (1) high estimate; (2) low estimate; and (3) best estimate of the relative catch of sand lance from a monitoring program in 25 years, as compared to today (Figure 1). Experts were also asked to provide an estimate between 50% and 100% for the confidence level associated with their intervals (Speirs-Bridge et al., 2010). To compare between experts, the lower and upper bounds were standardized to 90% credible intervals (Hemming et al., 2018).

Survey 3: review

Survey 3 provided an opportunity to review the results of the 2^nd Survey, including the comments and allow experts to finalize their estimates, adjusting if needed. Twenty-one experts completed Survey 3. We used the results of Survey 3 to calculate the final relative vulnerability assessments and as the final expert estimate of the population trajectory.

Results

Survey 1 – threat identification

Experts recommended 0 to 5 additional threats each. After accounting for duplicates, 34 additional threats were provided by the experts (Supplementary Table S2). When asked to broadly categorize the list of threats, participants placed as few as one and up to 23 in the Of Concern category (average of 10), zero to nine in the Least Concern category (average of three), and zero to 11 in the Uncertain category (average of seven). Climate change, followed by shoreline armoring were the most voted-for threats in the Of Concern category, with 31 and 30 total votes, respectively (Table 3). Recreational boating (14), commercial fishing (12), and recreational sites (11) were listed the most for threats of Least Concern. Under the Uncertain category, geoduck harvesting received the most votes (21), followed closely by renewable energy and construction (20), and commercial ship anchorages (19). Other threats with considerable uncertainty votes included major shipping and port developments (15), aquaculture (15), and freshwater dams (15). There were 19 threats that only received one vote, and most were additional threats provided by an expert and not seen by the remaining experts. The only way such a potential threat could have received more than one vote would be for two experts to identify the same threat independently.

The Cumulative Rank Scores (CRS) typically led to the same ranking as the number of votes a given threat received (Table 3). For example, climate change, followed by shoreline armoring, again scored the highest in the total CRS, with scores of 642 and 608, respectively. Some exceptions were: accidental spills (received 27 votes with a CRS of 479), and dredging (received 29 votes with a CRS of 473). However, there were only three threats with a lower CRS rank compared to the direct rank.

In the comments section, many participants addressed their lack of certainty with the threats and difficulty in ranking them. Several commented on how the spatiotemporal nature of a particular threat impacted their ranking choices, while others noted how their familiarity with a particular threat may have driven their rankings. Others commented they were not able to rank the threats without additional information given differences in scale among threats. Several participants with geology backgrounds pointed out that natural impacts such as earthquakes or shifts in geophysical processes may also have impacts on sand lance habitats. Several participants commented on confusion or specific concerns they had with certain threats, or how the threats were categorized. These comments were used to refine the final threats list and description of threats for Survey 2 (Tables 3, 4).

Survey 2 and 3: vulnerability assessment and expert population trajectory

Vulnerability assessment

The vulnerability assessment was completed by 30 experts; however, 5 abstained from providing estimates. Group A had 18 experts, and Group B had 12. In Survey 3, one expert altered just one of their responses to the vulnerability matrix table. This expert changed their response regarding the duration of shoreline armoring from (4) 1-10 years, to a higher value of (5) 10-20 years, changing the overall average from 5.78 to 5.8. The results presented are the final judgements by participants. The average of expert’s vulnerability score, the order of the relative vulnerability, and the most imminent threats scores were estimated to be (in order of highest to least): sea level rise, sea temperature rise, extreme weather, ocean acidification, decreased sediment loads from freshwater sources, and shoreline armoring (Figure 2). Aquaculture of kelp, salmon, and shellfish had the lowest scores.

Figure 2

The vulnerability scores were then disaggregated into area, duration, and occurrence (Figure 3); resistance (Figure 2); and certainty (Figure 4) and ordered according to the vulnerability scores, from highest to least (Figure 5). The resistance values roughly approximate the vulnerability scores, likely because of the higher weight this criterion was given relative to other criteria. However, duration, area, and frequency contribute to variability in these rankings. For example, climate change threats made up four of the top five threats in the overall relative vulnerability scores (Figure 5), but they were not always the top scoring resistance values (Figure 2). On average, experts thought sand lance are betterfrmoval) had the lowest median resistance value (3.2, Figure 2). Dredging had relatively low occurrence values, at least once per year (1.78, Figure 3A), meaning experts think sand lance and sand habitat are poorly able to cope with the impacts of dredging; however, they also thought this threat does not occur as often as other threats. At the other end of the threats assessed, kelp aquaculture had the lowest relative vulnerability score, and the lowest resistance values (0.6, Figure 2), but the highest occurrence value (6, Figure 3A), with moderate duration and area values. Certainty values varied little among threats, approximately 2, and made very little difference to the rankings of threats.

Figure 3

Figure 4

Figure 5

Population assessment

Only five participants (of 30) declined to estimate the population trajectory (declining to answer each of three population questions). The results of the remaining 25 experts suggest that, on average, sand lance are expected to decline to 63% [95%CI: 20.1 – 185.5] of today’s population under a ‘business as usual’ scenario (Figure 6). While the upper and lower bound on this estimate exhibited high uncertainty, we note that only one participant (3%) estimated the population to increase, and three (9%) estimated it would remain the same. Many experts (40%) commented that they based their population projection estimate on assumptions that are supported in the literature, including anecdotal observations that suitable shoreline habitats are increasingly impacted or lost, threat intensity and occurrence frequencies appear to be increasing, extirpation and extinctions of other species in the Salish Sea are occurring at a rapid rate, and that ecosystem processes are decaying (Pimm et al., 2014; Díaz et al., 2019; Chase et al., 2020; Arimitsu et al., 2021; Laubenstein et al., 2023). The single expert that estimated a population increase cited that sand lance are a resistant species despite the habitat damage and loss, and changing climate conditions.

Figure 6

Three participants made changes in the follow-up survey after discussing initial results with other experts. There were two participants that changed their population trajectory assessment and widened their bounds (decreased their certainty), one also lowered their best guess. These changes made the overall average slightly lower and the bounds slightly wider.

Discussion

We present the first Salish Sea-wide evaluation of expert-based sand lance population trajectory, as well as the most comprehensive threat and vulnerability assessment conducted for the species to date.

Threats

The vulnerability assessment gathered experts from a wide range for backgrounds to carefully garner (1) a comprehensive list of threats to Salish Sea sand lance (Supplementary Material S1), (2) a list of the most concerning threats, and (3) prioritization of these top threats (Figures 2–6). The results indicate that sand lance are considered most vulnerable to climate change, which was thought to be a major threat to sandy beach habitats since the early 2000s (Brown and McLachlan, 2002). There is some existing research that specifically supports the notion that climate change poses a significant threat to sand lance populations. For example, a number of studies assessing sand lance mean body weight, size, condition, and fat content all negatively correlate with periods of increased temperatures (e.g., marine heat waves, Robards et al., 2002; Hipfner et al., 2018; von Biela et al., 2019; Arimitsu et al., 2021; Robinson et al., 2023). In addition, lab research on ocean acidification impacts to Ammodytes dubius, a species within the same genus occurring in the Northwest Atlantic, showed A. dubius eggs are highly sensitive to changes in CO₂ at levels within the range of expected climate change values (Murray et al., 2019; Baumann et al., 2022). Finally, sea level rise is also projected to influence tidal currents, which may lead to the erosion and loss of sand, endangering rare shoreline and subtidal sand lance habitats (Healy, 1996; Greene et al., 2017; Greene et al., 2021).

While mitigation measures for climate change require national and global scale efforts, other threats (e.g., sediment loads, shoreline armoring and pollution) can be abated through local regulatory and/pr policy decisions of the Salish Sea (e.g., those approving permits for development or dredging). Shoreline armoring was among the top-ranked threats in the initial survey and has been of high concern amongst conservation groups since the early 2000s (de Graaf, 2010; Hart, 2010; de Graaf, 2014, 2017). Of the top threats, changes to sediment loads (e.g. such as that from dams or shoreline development) and shoreline armoring may be easier to address relative to the multifaceted, global nature of climate change (Hornsey and Fielding, 2019; Habel et al., 2020; Toft et al., 2021). Addressing local impacts, such as damage or loss of crucial spawning habitat, would contribute to offsetting complex threats such as sea level rise, sea temperature rise, pollution, and marine riparian area loss. There is mounting evidence of the benefits of dam removal which returns natural sediment regimes (Frick et al., 2022; Shaffer et al., 2023), avoiding shoreline armoring in favor of restoring and maintaining the natural capacity of nature to buffer adverse impacts using natural shoreline designs (Brown and McLachlan, 2002; Gittman et al., 2016; Martin and Watson, 2016), and avoiding dredging (Wenger et al., 2017).

While our assessment focused on threats to sand lance, we note that many of the top-ranked threats have been previously highlighted as key issues for other species and across ecosystems (Halpern et al., 2007; Crain et al., 2009; Defeo et al., 2009; Teck et al., 2010; Gaydos et al., 2015). They are also likely to be applicable to species that use the same habitats as sand lance, and for the predators that depend on them (Beaudreau and Essington, 2007; Defeo et al., 2009; Page et al., 2011; The Salish Sea Pacific Herring Assessment and Management Strategy Team, 2018; Smith and Liedtke, 2022). Therefore, applying a threat-based approach to management of sand lance habitats, such as a priority threat management plan (Martin et al., 2018), could provide an efficient means of safeguarding multiple species facing the same threats.

The threat assessment revealed that there is still much uncertainty about many threats, with 28 threats grouped as uncertain, and differences among experts in how they ranked threats. This is not surprising given the lack of research on this species and habitat. The uncertainty in the vulnerability matrix and comments provided by experts identifies collective gaps for future research (Supplementary Materials, Survey 2 Results Summary). While the threat assessment revealed many potential threats acting on sand lance, the average resistance value was ‘moderate’, suggesting sand lance may be resilient in the face of many threats. This result was echoed by several expert comments. This may explain the more optimistic predictions for population trajectory from some experts. Perhaps the secret to sand lance resilience is buried in their life history. Sand lance are more dormant throughout the later fall and winter months buried in sandy substrates, and, during this period, they regrow gonads in preparation for annual spawning (van Deurs et al., 2010; Zhukova and Baker, 2022). Mature sand eels in the North Sea are known to balance the increased metabolic costs of warm years with reduced gonad mass, which may buffer the effects of poor environmental conditions (Wright et al., 2017). Throughout marine heat wave years, when sea temperatures were above average for extended periods and zooplankton communities (prey) were altered, sand lance in Alaska (A. personatus) responded by burying more (Arimitsu et al., 2021). Researchers suggested that these sand lance may have adjusted daily and seasonal dormancy periods to reduce metabolic costs associated with warmer water temperatures, and subsequently thrived (Arimitsu et al., 2021). While sand lance may display resistance, their body condition, and thus nutritional value for predators, significantly declines during periods of warm ocean conditions, and/or when prey communities are altered (Litzow, 2000; Robards et al., 2002; von Biela et al., 2019; Robinson et al., 2023). This double impact of reduced abundance and nutritional value of sand lance and other forage fishes (e.g., capelin, Pacific herring, Pacific sardine, and northern anchovy) brought on by the 2014-2016 marine heat wave led to cascading impacts, shifting distributions, and resulting in large-scale mortality events of marine predators such as seabirds, marine mammals, and groundfish (Piatt et al., 2020; Arimitsu et al., 2021). Although sand lance populations may be resilient to climate change, it is not without any impact to the wider community.

Population

The experts interviewed in this study collectively suggest that sand lance populations in the Salish Sea could be 63% of what they are today (a 37% decline) in 25 years under current management scenarios. We acknowledge that there is much uncertainty around this population’s future status, which can be attributed to inherent biological attributes of forage fishes, a lack of wide scale, regularly occurring population surveys for sand lance, and a dearth of information about the direct impacts of specific threats on sand lance at both the individual and population levels. The expert projection contradicts the positive trend seen in the forage fish study across subbasins of Puget Sound using integrated trawl data (Greene et al., 2015). The authors of that study suggest that the differences in subbasin forage fish populations may be attributed to anthropogenic influences.

Our results highlight the need to better understand sand lance populations. A decline of the magnitude predicted by experts here would have ecosystem-wide implications particularly to predators that depend on sand lance during critical times in their life history (i.e., sea bird breeding) (Bertram and Kaiser, 1993; Bertram et al., 2001; Beaudreau and Essington, 2007; Gutowsky et al., 2009; Hipfner et al., 2018; Duguid, 2020). Given this species importance to the ecosystem and our collective interest in the economic and cultural values provided by top predators (e.g. salmon, orcas, lingcod, sea birds, etc.), we recommend the development and initiation of long-term, cross-border coordinated field-based population monitoring programs to address the hypothesis developed here that sand lance populations are in decline.

Method review

An additional benefit from this study is the progressive application of a method for assessing populations and threats together, and that these assessments may be applied to other cryptic species. The process applied here was collaborative, transboundary, and enabled information to be gathered from experts at a regional scale. The elicitation was relatively expedient, with results for 20 threats being obtained in three online surveys within 10 months. Experts provided 34 new threats that were not initially identified in the literature. While we did not quantify all threats with a vulnerability score, our list contains information on these threats. The framing of the elicitation question for the population status seemed to enable most experts (25 out of 30) to provide a best estimate of the expected trajectory of sand lance, and accompanying credible intervals, a response rate that surprised even the authors.

There are aspects of the approach applied here that might be improved for subsequent case studies. There were many decisions in the method development process, and we deliberated frequently over the best, or least-biased approach to acquire a truly relative comparison of the threats. On reflection, an additional initial survey to gather all the possible threats first, and then in a subsequent and separate survey to conduct a threat ranking activity would have allowed all experts to see the additional threats suggested by their peers. This would take additional time but may have reduced variability among experts.

Another improvement could be to hold a workshop to elicit which vulnerability criteria to use in the assessment, which would help better define criteria. This may lead to a more context-specific assessment process in which participants are more engaged (Stelzenmüller et al., 2018). Reassessing criteria weights used in the vulnerability calculation may also be warranted to have the best possible weighting specific to this context, area, and species and provide further expert engagement. Providing additional time for experts to spend thinking about the vulnerability criteria and the best threat weighting methodology may lead to better understanding of this complex concept and their application when accessing threats.

Defining terms was a difficult and time-demanding task. Even though attention was given to providing careful definitions, experts may have interpreted the threats differently, which may have contributed to some of the highly variable vulnerability scores. Linguistic uncertainty is a common issue in expert elicitation (Hemming et al., 2018) and underscores the importance of allowing experts to review and update their judgements, which can help to reveal and resolve uncertainties caused by ambiguity.

We faced a trade-off in mental load (how many threats we asked experts to evaluate) and the quality of their answers (e.g., was 10 threats too many or sufficient)?. One expert objected to leaving a particular threat out that they thought was important. Increasing collaboration and opportunities to review and change the list of threats may have addressed these concerns. To guard against a high non-response rate, we deliberately had large groups. Given the high response by experts, it may be possible to have assessed vulnerability for more threats, or to have split the experts into smaller groups of 5-8 experts to assess more of the threats.

Finally, many of the top threats identified (Table 4) occur over long time scales, and have both direct impacts on individuals as well as indirect impacts on sand lance habitat or food webs. Almost certainly, these threats interact, overlap, and amplify one another (Crain et al., 2008; Laubenstein et al., 2023). Although investigating the interactions was beyond the scope of this study, understanding if and how threats individually drive population responses and interact (e.g., acidification and warming; [Crain et al., 2008)] would help interpret and predict cumulative interactions.

Conclusion

Using expert elicitation, we gathered information on an understudied and difficult to study species, Pacific sand lance, in an efficient and low-cost manner. Expert opinion predict a decline in sand lance abundance in the Salish Sea under a business-as-usual scenario, highlighting the need for further investigation into Salish Sea sand lance populations and their persistence. A decline in sand lance abundance would have major cascading effects throughout the Pacific coastal ecosystem. The top threats identified include climate change, nearshore development, and pollution. Addressing knowledge gaps identified here to improve conservation decisions is one step toward a more sustainable, sand lance-abundant coast.

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