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Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Journal of Environmental Management 91 (2010) 2771e2780 Contents lists available at ScienceDirect Journal of Environmental Management journal homepage: www.elsevier.com/locate/jenvman Vulnerability of Fraser River sockeye salmon to climate change: A life cycle perspective using expert judgments Tim McDaniels a, *, Sarah Wilmot b, Michael Healey c,1, Scott Hinch d, 2 a Institute for Resources, Environment and Sustainability at the University of British Columbia, Lasserre Building, 433 e 6333 Memorial Road, Vancouver, BC Canada V6T 1Z4 School of Community & Regional Planning at the University of British Columbia, 433-6333 Memorial Road, Vancouver, BC Canada V6T 1Z2 c Institute for Resources, Environment and Sustainability at the University of British Columbia, Aquatic Ecosystem Research Laboratory, 432 e 2202 Main Mall, Vancouver, BC Canada V6T 1Z4 d Institute for Resources, Environment and Sustainability, University of British Columbia, 1933 West Mall Vancouver, BC Canada V6T 1Z4 b a r t i c l e i n f o a b s t r a c t Article history: Received 24 June 2009 Received in revised form 12 July 2010 Accepted 7 August 2010 Fraser River sockeye salmon have been the basis for a major commercial fishery shared by Canada and the United States, and an important cultural foundation for many aboriginal groups; they are also of huge ecological significance throughout the Fraser Basin. The potential for altered aquatic habitat and temperature regimes due to climate change is an important concern for Fraser River sockeye salmon. This paper characterizes the vulnerability of Fraser River sockeye salmon to future climate change using an approach that is novel on three counts. First, previous efforts to assess the vulnerability of salmon to climate change have largely focused on only part of the life cycle, whereas we consider climate vulnerability at all stages in the life cycle. Second, we use the available scientific literature to provide a basis for structuring and eliciting judgments from fisheries science and management experts who research and manage these systems. Third, we consider prospects for mitigating the effects of climate change on sockeye salmon. Tests showed that participants’ judgments differentiated in statistically significant ways among questions that varied in terms of life stages, spawning regions and climate scenarios. The consensus among participants was that Fraser River sockeye are most vulnerable to climate change during the egg and returning adult stages of the life cycle. A high temperature scenario was seen as imposing the greatest risk on sockeye stocks, particularly those that migrate to the upper reaches of the Fraser River system and spawn earlier in the summer. The inability to alter water temperature and the highly constrained nature of sockeye management, with competing gear types and sequential fisheries over a long distance, suggest the potential to mitigate adverse effects is limited. Fraser River sockeye already demonstrate a great deal of adaptive capacity in utilizing heterogeneous habitats in different river sub-basins. This adaptability points to the potential value of policies to make stocks more resilient to uncertain futures. Ó 2010 Elsevier Ltd. All rights reserved. Keywords: Climate change Sockeye salmon Characterizing vulnerability Life cycle stages Participant judgments 1. Introduction The Fraser River has been described as the most important salmonine-producing river system in North America (Northcote and Larkin, 1989). Sockeye salmon (Oncorhynchus nerka) are the second most abundant salmon species in the Fraser River, after pink salmon (O. gorbusha), which have a much lower economic value. * Corresponding author. Tel.: þ1 604 822 9288; fax: þ1 604 822 3787. E-mail addresses: timmcd@interchange.ubc.ca (T. McDaniels), healey@ interchange.ubc.ca (M. Healey), shinch@interchange.ubc.ca (S. Hinch). 1 Tel.: þ1 604-822-4705; fax: þ1 604-822-9250. 2 Tel.: þ1 604-822-9377; fax: þ1 604-822-9102. 0301-4797/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jenvman.2010.08.004 The fishery for Fraser River sockeye salmon has been the most economically valuable commercial salmon fishery in Canada, shared with fishers from the United States under the Pacific Salmon Treaty (Williams, 2007). Aboriginal communities depend on the sockeye runs to provide salmon for food and ceremonial purposes (Jones et al., 2004). Sockeye salmon migrate to spawning beds distributed from near the river mouth to more than 1000 km upstream in important tributaries in the Fraser system (Northcote and Larkin, 1989), providing protein and nutrients through much of the 230,000 km2 of the Fraser basin (Finney et al., 2000; Helfield and Naiman, 2001; Johnston et al., 2004). In recent years, production of Fraser sockeye has declined precipitously and it was recently classified as ‘endangered’ by the IUCN in the first ever global endangerment assessment on Author's personal copy 2772 T. McDaniels et al. / Journal of Environmental Management 91 (2010) 2771e2780 a salmonid (IUCN-SSG, 2009). There are many hypotheses for the causes of this decline, including freshwater and ocean habitat changes, over-fishing, diseases, and other factors, all of which were recently evaluated by a ‘think tank of sockeye experts’ (STTS, 2009). In 2010, the issue is being evaluated by a federal judicial inquiry (the ‘Cohen Inquiry’). Global climate change is likely playing a large role in this decline. Various authors have examined the potential impact of global climate change on particular life stages of sockeye salmon, with many of the analyses done on Fraser sockeye stocks (e.g., Henderson et al., 1992; Hinch et al., 1995a, 1995b; Swansburg et al., 2002; Rand et al., 2006; Farrell et al., 2008; Hague et al., in press; Martins et al., in press), as well as on overall production rates (e.g., Klyashtorin, 1998; Levin, 2003), and concluded that Fraser sockeye salmon would experience declining production based on recent changes in climate, and production would continue to decline as climates continue to change. The objective of this paper is to characterize the vulnerability of Fraser River sockeye salmon to future climate change. Its approach is novel on three counts. First, previous efforts to consider vulnerability of sockeye salmon to climate change have generally only focused on part of the life cycle (e.g., Hinch et al., 1995b; Henderson et al., 1992; Rand et al., 2006), although numerous studies have considered Chinook, Atlantic salmon, and steelhead (e.g., Crozier et al., 2008; Mangel, 1994). Pacific salmon are anadromous, occupying various fresh water and marine environments at different life stages. Hence, over their life cycle, sockeye salmon integrate the effects of climate change on fresh water and marine ecosystems, and the consequences for one generation can carry forward to influence reproductive success, abundance and ecological fitness in subsequent generations. To date, no study has examined the way changes at one life stage propagate through the life cycle to affect other stages or accumulate across generations (Healey, submitted for publication). Here we consider the effects of climate change on the vulnerability of sockeye salmon to changing habitat at all life stages. Second, while expert judgments are used extensively in risk and decision analysis, often in the form of elicited probabilities of specific events, the approach adapted here is novel in considering vulnerability over life cycle stages, climate scenarios and regions of the Fraser River system. Third, we also consider prospects for mitigating the effects of climate change on sockeye salmon. 2. Scientific understanding regarding climate change and Fraser sockeye 2.1. Sockeye salmon abundance cycles and recent changes Fraser River sockeye populations are characterized by a 4-year cycle of abundance with one or two years in four having much greater abundance than others (Burgner, 1991). The causes of this cycle remain unknown (Ricker, 1997). Fraser sockeye also fluctuate in abundance in relation to decades-long cycles in ocean environmental conditions (Mantua et al., 1997 discusses this pattern for Pacific salmon in general). Presumably in response to one of these oceanic regime changes, Fraser River sockeye began increasing in abundance dramatically at the end of the 1970s, reaching historic high abundance in the mid 1990s. After 1995, abundance in terms of annual harvest surplus began to decline, in coincidence with changes in ocean conditions (M. Lapointe, pers. comm.). Pacific salmon populations, living near the southern extent of their range in the Columbia River and Fraser River, have all experienced significant increases in summer freshwater temperatures since the 1950s (Patterson et al., 2007; Crozier et al., 2008) and such increases during spawning migrations have been identified as a major threat to the future viability of salmon populations in both the Columbia and Fraser River systems (Rand et al., 2006; Farrell et al., 2008). Indeed, several studies have quantified a negative relationship between episodes of unusually warm river temperatures and salmon health and mortality (Naughton et al., 2005; Young et al., 2006; Patterson et al., 2007; Crossin et al., 2008; Mathes et al., 2010). Most of the 150 stocks (i.e. populations) in the Fraser River initiate adult river migrations between July and October, encountering a range of temperatures. The 40-year average daily temperature is lowest in July and October (w15 C), and highest in August (w19 C; Patterson et al., 2007). The Fraser River has experienced an average increase in peak summer water temperature of >1.5 C over the past 40 years. Eight of the past 10 summers (as of 2009) have been the warmest on record (Morrison et al., 2002). Thus, all stocks now encounter warmer river temperatures than they once did, and, one group of stocks, the Late-runs, which includes the world-famous Adams run, encounter temperatures 3e6 C warmer than historic. This has occurred because, since 1994, Late-runs have begun entering the Fraser River 2e6 weeks earlier than normal (Cooke et al., 2004). While the causes of this phenomenon are not clear, evidence suggests that changes in ocean environments and endogenous migratory cues are responsible (Hinch and Gardner, 2009). Early migrating Late-run adult sockeye experience 50e95% mortality prior to spawning (Cooke et al., 2004; Hinch and Gardner, 2009) and the causes of mortality have been shown to be related to the higher migratory temperatures encountered (Crossin et al., 2008; Mathes et al., 2010). Other Fraser runs of sockeye are also perishing at relatively high levels when river temperatures are relatively warm (Martins et al., in press). Because Late-runs have changed their river entry timing, and because the Fraser River is much warmer in summer now than in the past, segments of all Fraser River sockeye stocks now encounter river temperatures >19 C during a portion of upstream migration. This change has profound evolutionary significance because no sockeye stock anywhere in the world is known to have initiated river migration at 20 C (Hodgson and Quinn, 2002). River temperature is therefore an important factor in the search for causes of the current declines in stock abundance (Crossin et al., 2008). 2.2. Sockeye salmon life cycle Sockeye salmon are anadromous and semelparous. Young spend one to several years in freshwater before migrating to sea where they grow to adult size and return to their natal stream to spawn (Burgner, 1991). For the purposes of this paper, we distinguish among eight stages in the sockeye life cycle. The rationale for eight stages rather than the more traditional five is to address migrational life stages (Hinch et al., 2006). Different stages require different habitat, as shown in Table 1. Details on life-stage specific movements and migrations for sockeye salmon can be found in Hinch et al. (2006). Table 1 Life cycle stages of Sockeye salmon. Life cycle stage Habitat Egg Fry e emergence to lake entry Fry e lake entry to first winter Fry e first winter Fry e smolt Post smolts Immatures Returning adults Fresh water (lakes and rivers) Fresh water (lakes and rivers) Fresh water (lakes and rivers) Fresh water (lakes and rivers) Fresh water, moving towards ocean Estuary and coastal ocean Ocean Ocean, coastal, estuary, and fresh water rivers and lakes Author's personal copy T. McDaniels et al. / Journal of Environmental Management 91 (2010) 2771e2780 For this study we grouped Fraser River sockeye stocks into three broad categories based on the location of their spawning grounds along the Fraser River: upper (northern), middle, and lower (southern). These three groups of stocks generally return to the river at different times, have different cycles of abundance, and occupy different habitats during the fresh water life cycle stages shown in Table 1. Our classification scheme creates some unavoidable overlap among groups in some of these variables. 2.3. Environmental changes caused by climate change that may affect Fraser River sockeye Global climate change is expected to result in higher average temperatures and altered precipitation patterns in the Fraser River basin, which will alter the habitat for sockeye salmon throughout their life cycle stages. The Pacific Climate Impacts Consortium provides access to a range of climate change scenarios for the Fraser Basin, drawing on various global circulation models (GCMs) and future greenhouse gas emission scenarios. There is a high level of uncertainty within and among the scenarios and models, although all indicate warmer air temperatures and changes in precipitation patterns. Over all scenarios of emissions and economic activities, and over all models, estimates of average annual increase in air temperature for the Fraser Basin by 2070 range from about 2.5 C to about 5.5 C compared to the average for 1980 to 1999 (PCIC, 2008). Hydrological models for the Fraser River predict earlier peak summer water temperatures with a 2e4 C average warming of the Fraser River over the next few decades, relative to temperatures experienced in the 1990s (Morrison et al., 2002; Rand et al., 2006; Ferrari et al., 2007; Hague et al., in press). Detailed analyses have been conducted to assess likely changes in Fraser River flow and temperature patterns. Morrison et al. (2002), using historic data from the past 50 years, found that summer temperatures have been increasing and peak flows decreasing. Based on GCM predictions, these trends are expected to continue. Specifically, for the period 2070e2099, the flow model predicted a modest 5% (150 m3/s) average flow increase but a decrease in the average peak flow of about 18% (1600 m3/s). These peaks would occur, on average, 24 days earlier in the year, even 2773 though for 13% of the years, the peak flow would occur much later as a result of summer or fall rain, instead of the currently normal spring freshet. In the same period, the summer mean water temperature is predicted to increase by 1.9 C. As a result of these changes in flow, freshwater spawning and rearing areas are expected to change. Using output from GCMs in conjunction with empirical time-series analyses of hydrologic data, Moore (1991) and Levy (1992) argued that within the next 80e100 years, the streams, lakes and groundwater in the Fraser Basin will warm by 1e4 C; there will be an increase in stream velocities in winter and spring though a decrease in summer and fall precipitation, and earlier spring freshets. Altered runoff patterns are predicted to make the Fraser River drainage more oligotrophic, resulting in a reduction in the abundance and availability of food for juvenile sockeye, which are reared in lakes (Henderson et al., 1992). Key environmental features in the North Pacific Ocean are also expected to change. Simulation results from GCMs, coupled with a simplified mixed-layer ocean model, predict that within the next 80e100 years sea surface temperatures will warm 2e4 C, and north-south air pressure gradients will weaken, leading to reductions in surface winds and wind-driven upwelling, as well as a 5e9% decrease in zooplankton biomass food production for ocean sockeye (Hinch et al., 1995b). The broad potential impacts of climate change on sockeye habitat in the Fraser Basin are summarized in Table 2. 3. Method 3.1. Role of judgments from scientific and management specialists Any method for assessing and managing risks will necessarily rely on the informed judgments of technical specialists and scientists to some extent. Methods have been developed and applied to characterize judgments about uncertainties in the form of probabilities for specific well-defined events (Keeney and von Winterfeldt, 1986, 1989; Morgan and Henrion, 1990). Probability elicitation has been employed in various climate change contexts, including, for example, changes in ocean circulation patterns (Zickfeld et al., 2007). However, these methods are time intensive, Table 2 Broad potential impacts of climate change on fraser basin sockeye habitat. Habitat Spawning streams during spawning and incubation Nursery lakes Coastal marine habitats Gulf of Alaska Sources: See details and references in Healey (2010). Impact of climate change Spawning streams will be warmer during the normal late summer/autumn spawning time and through the incubation period. Spring freshet will be earlier and may be of shorter duration due to the decrease in snow pack. Discharge may be somewhat lower in later summer/autumn but may remain higher over the winter if more winter precipitation falls as rain. Coastal spawning streams will be warmer and may be subject to stronger winter freshet if winter storms intensify. Temperatures in summer will be higher, particularly in smaller streams, which may cause stress for stream resident species like coho (Oncorhynchus kisutch) and Chinook (Oncorhynchus tschawytscha) but may be less important for migratory species such as sockeye. Interior lakes will lose ice cover earlier in the year (or may not be ice covered at all), may stratify thermally earlier and remain stratified longer and will have higher summer epilimnion temperatures. Coastal nursery lakes may also stratify longer and have higher summer temperatures. Coastal waters of British Columbia will be warmer and productivity will probably be higher. Spring plankton blooms will probably occur earlier. Along the coast of Alaska, where downwelling conditions occur, there may be nutrient limitation due to reduced upwelling in the central Gulf of Alaska. Surface temperatures will be warmer and gyre circulation may be slower due to weakening of the Aleutian low. Upwelling may be reduced and production lower. Author's personal copy 2774 T. McDaniels et al. / Journal of Environmental Management 91 (2010) 2771e2780 require extensive commitment from those who provide the judgments, and typically only focus on one variable at a time. Other approaches to eliciting judgments include seeking consensus among a nominated group through iterative responses to specific questions (e.g., the Delphi method) (Linstone and Turoff, 1975), or consensus reports derived through negotiation and review, such as the Intergovernmental Panel on Climate Change (IPCC, 2007). In the present study the concern is with interactions over a wide range of variables (eight different life stages, three regions, and two climate regimes). Hence, a judgment-based approach was used to characterize vulnerability to climate change, but not in probabilistic terms. Unlike some of the approaches noted above, we also saw no reason to force a consensus in the judgment process, through iteration or negotiation, because previous studies have shown that consensus approaches narrow the range of differences among expert views (Morgan and Henrion, 1990). Hence, we sought an approach that could be implemented in a group context, allowing for individual expression of views, followed by interpretation over the opinions of recognized experts on Fraser River sockeye salmon and climate change. 3.2. Characterizing scientific knowledge Three approaches were used in this research to structure scientific knowledge and thus provide the basis for the judgmental assessment of vulnerability. First, interviews were conducted with scientific specialists, including two of the authors of this paper (Authors’ names deleted), to confirm that considering sockeye salmon vulnerability to climate change throughout their whole life cycle is sensible and relevant as a basis for structuring vulnerability judgments, and that managers and scientists would want to consider the vulnerability of specific geographic groups of Fraser River sockeye stocks. Second, an extensive background paper was prepared summarizing available scientific information regarding the effects of climate change on sockeye (Author’s name deleted). The information was structured in terms of a conceptual model that considers how changes to sockeye due to climate change at one life stage may propagate through the life cycle to affect other stages or accumulate across generations. The paper also included a series of influence diagrams (Howard, 1989; Clemen and Reilly, 2000) illustrating possible linkages among variables that could influence the possible effects of climate change on each life cycle stage (Fig. 1 provides one example). The figures are not deterministic, nor do they imply the linkages necessarily hold. They are representations of beliefs in the form of a model on paper. The third step was the creation and testing of a survey instrument that was meaningful for the participants, and workable in terms of the tasks required. This survey instrument is described below. 3.3. Participants Selecting participants for an expert elicitation is not a matter of random sampling within a sampling frame. Rather it is a process of recruiting the most knowledgeable people about the technical issues at hand, while recognizing the range of thinking about these issues. We had a two-stage process to select participants. First, the fisheries specialists on the study team nominated individuals recognized as highly knowledgeable about sockeye salmon and climate issues. Second, some of those individuals nominated other participants. A one-day workshop was held in December 2006 to obtain judgments regarding sockeye vulnerability. Participants included academic scientists, federal and provincial government staff members, and non-government organization staff members knowledgeable about Fraser River sockeye and climate change. Confirmed attendees were sent the background paper so they could become familiar with the available literature prior to the workshop. Thirteen experts participated in the workshop (seven categorized themselves as biologists, four as policy makers, one as “both”, and one as “neither”).1 The mean number of years of experience was over 16, with the biologists having more experience (20 years) on average than the policy-makers (7 years). 3.4. Structure and survey instrument design The workshop began with brief presentations on key topics (including an overview of the literature on likely environmental trends given climate changes) to ensure participants understood the tasks. Vulnerability was defined as “.the extent to which a natural or social system is susceptible to sustaining damage from climate change. Vulnerability is a function of the sensitivity of a system to changes in climate and the ability to adapt the system to changes in climate. Under this framework, a highly vulnerable system would be one that is highly sensitive to modest changes in climate.” (IPCC 1997 definition cited by The Vulnerability Network, http://www.vulnerabilitynet.org/) For the first half of the workshop, participants used a workbook to rate: 1) the vulnerability of sockeye at each life stage, 2) the vulnerability of sockeye over their entire life cycle (overall vulnerability); and 3) the participant’s knowledge and confidence regarding the previous two exercises. Participants were given the opportunity to discuss their responses and adjust their answers if their opinions changed as a result of the discussion. The questions were designed so that responses could be analyzed for differences between the life cycle stages, between the individual stages, and overall. Pre-defined scales were used to describe various levels of vulnerability and the same scale was used for all questions. A sample question is shown in Fig. 2 for one geographic area. 3.5. Structuring the judgments The questions elicited judgments of vulnerability in relation to life stage, spawning region, and climate forecast. The first set of questions asked participants to rate the vulnerability of sockeye at each life stage under two different climate change scenarios (2 C and 4 C average air temperature increases), and for three separate spawning regions (upper, mid and lower Fraser River). This created a total of six combinations. The two scenarios were cast as a relatively low and relatively high temperature increase, reflecting a likely minimum and maximum range based on the available literature for the Fraser Basin and North East Pacific Ocean (Moore, 1991; Henderson et al., 1992; Levy, 1992; Hinch et al., 1995b; Morrison et al., 2002; PCIC, 2008). Clearly, there are many environmental changes associated with these temperature changes (e.g., a rise in river temperature is associated with a decrease in river discharge; a rise in ocean temperature is associated with a decrease in wind strengths and upwelling). Overall, the more extreme the change in temperature, the more extreme would be the expected change in the associated environmental features. We asked participants to consider the temperature change as an indicator of the myriad of environmental changes that may occur simultaneously with temperature changes. Nonetheless, temperature changes are expected to have some of the most direct and dramatic effects on salmonids. The accuracy of the 2 C and 4 C scenarios was not the concern of this workshop, which focused 1 The individual self-identified as neither a biologist nor a manager is a former federal Minister of Fisheries, and a knowledgeable member of non-governmental organizations regarding fisheries issues. Author's personal copy T. McDaniels et al. / Journal of Environmental Management 91 (2010) 2771e2780 2775 Fig. 1. Sample influence diagram (returning adults life cycle stage). instead on how vulnerable sockeye were to adverse effects given these two reasonably understandable scenarios. Participants were asked to consider the effects over a 60-year time frame (15 cycles of sockeye salmon), and to consider the effects summarized in Table 2 all together. The questions were organized by life cycle stage and the issue of vulnerability focused on the ability of the sockeye to move on to the next stage of their life cycle in good state (i.e. considering both quantity and quality) under each climate scenario. Participants circled a number between 1 and 5, where 1 indicated no vulnerability (i.e. no different from the status quo) and 5 indicated a high degree of vulnerability (i.e. reproductive capacity is severely disrupted). The second exercise asked the participants to rank the overall vulnerability of sockeye salmon (on the same 1e5 vulnerability scale) to 2 C or 4 C climate warming in each of the three regions over the same 60-year time frame. Answers to this question were later compared to the answers for individual life cycle stages. Finally, participants were asked to rate their knowledge of and confidence in their responses to each question. 3.6. Eliciting and revising judgments All judgments for a particular life stage were elicited together, for both temperature scenarios and for the three spawning regions. Before each life stage was considered we reviewed the structure of the influence diagram and content of the background paper relevant for that question. After all participants had completed their judgments for a given set of questions, we encouraged participants to discuss their answers. For some life cycle stages, lively discussion ensued, and for others, little was said. Participants were permitted to revise their judgments at any time. A review of the workbooks showed that 11 of the 13 participants had revised at least one answer; some had made many revisions. 3.7. Statistical approach After the workshop was completed, responses to the questions were compiled in a database. We used the non-parametric Author's personal copy 2776 T. McDaniels et al. / Journal of Environmental Management 91 (2010) 2771e2780 Fry Emergence to Lake Entry As described above, the faster development of embryos may lead to early emergence of smaller fry. This early emergence may result in a mismatched timing with the spring bloom of zooplankton. This mismatch may limit feeding and growth opportunities for sockeye. When the nursery lake is upstream, fry must migrate against the current. Smaller fry may be less able to make such an upstream migration successfully. As a result, the quantity and/or quality of sockeye at the end of this lifecycle stage would be impaired. How vulnerable are fry, from their emergence to lake entry, to this reduction in quantity and/or quality? Sockeye the spawn in the upper Fraser system Vulnerability with 2ºC average temperature increase 1 2 3 4 Not vulnerable (not affected at all or status quo) 5 Highly vulnerable (reproductive capacity severely disrupted) Vulnerability with 4ºC average temperature increase 1 2 3 4 Not vulnerable (not affected at all or status quo) 5 Highly vulnerable (reproductive capacity severely disrupted) Fig. 2. Sample question for one life cycle stage and one spawning region. ManneWhitney U rank sum test to compare the distribution of responses for pairs of questions or question sets assuming a null hypothesis of no difference in the ranks (n ¼ 13)2. We conducted three sets of ManneWhitney tests. To investigate differences between life cycle stages when other variables were held constant, we compared vulnerability estimates for three life cycle stages (eggs, fry-first winter and returning adults) within all six temperature-region combinations.3 For example, we compared the vulnerability of the eggs life cycle stage in the upper Fraser region under a 2 C temperature increase scenario with the vulnerability of the fry-first winter life stage and the returning adults life cycle stage in the same region and at the same temperature increase. This analysis involved a total of 18 ManneWhitney tests (three for each of the six temperature-region combinations). To investigate differences between temperature scenarios and regions, we compared overall vulnerability estimates for the six combinations of spawning region and temperature increase. The overall vulnerability estimates for a particular temperature scenario and region were compared to the overall vulnerability estimates for the same region but at the other temperature. The overall vulnerability for a particular temperature and region was also compared to the same temperature in different regions. These tests investigated the impact of changing the location and temperature scenario on overall vulnerability. The third set of ManneWhitney tests investigated differences in knowledge and confidence of the participants for three life stages (eggs, fry-first winter, and returning adults). 2 A total of 63 data points out of the potential total of 936 were missing because some participants did not answer certain questions. Of these, 46 were left blank by one individual, who self-identified as a policy maker and not a fisheries expert. We handled these missing responses by replacing them with the mode response for that question, in keeping with the ordinal, categorical data structure. 3 We selected these three life stages for comparison because, a priori, they seemed to have the most potential to be affected by climate change. 4. Results 4.1. Histograms of the responses for each question Fig. 3 shows the histograms of responses for all questions. The histograms are all unimodal. The variation ranged from questions for which responses were in two adjacent categories (indicating high agreement) to questions for which responses were spread over four categories.4 The judgments showing high agreement (varying over only two categories) and high vulnerability of stocks were (i) eggs in the mid-Fraser under the 4 C scenario, and (ii) upper Fraser stocks over the whole life cycle under the 4 C scenario. Visual inspection of the histograms does not show that participants were more confident regarding the impact of a 4 C increase than of a 2 C increase, nor do they appear to be more confident about vulnerability over the entire life cycle than for any specific stage. 4.2. Life cycle vulnerability ratings Participants rated sockeye as most vulnerable to climate change during egg and returning adult life stages. Eggs had a mean score of 3.67 and returning adults had a mean score of 3.82 (for all regions and temperature scenarios). Mid-life cycle stages such as fry-first winter had, in contrast, lower vulnerability means (range 2.58e3.13). The means for each life cycle stage are shown in Table 3, broken out by location and temperature scenario, and shown for each life stage overall. The difference in vulnerability between eggs and fry-first winter was statistically significant (p < 0.01) for all six combinations of spawning region and temperature increase. None of the differences 4 In the two judgment sets for returning adults spawning in the Middle Fraser region, one participant judged vulnerability much lower than the other participants (Fig. 3, centre two histograms for returning adults). Author's personal copy T. McDaniels et al. / Journal of Environmental Management 91 (2010) 2771e2780 2777 Fig. 3. Histograms of responses for each question. in vulnerability between egg and other life stages were statistically significant. Likewise, the difference in vulnerability between the returning adults and fry-first winter stages was statistically significant (p < 0.01) for all six regionetemperature combinations. The difference in vulnerability between returning adults and fry-smolt was significant for the upper Fraser at 2 C and 4 C, and the lower Fraser at 2 C. None of the other differences in vulnerability were statistically significant. The mean vulnerability scores of the most vulnerable life stages (eggs and returning adults) were not statistically different from the mean score for the overall life cycle. 4.3. Overall vulnerability ratings Table 4 shows the mean ratings for overall vulnerability. Sockeye were viewed as substantially more vulnerable to climate change under the 4 C temperature scenario compared to the 2 C scenario. Table 3 Vulnerability (on a scale of 1e5) of upper, mid, and lower sockeye salmon at different temperatures and by life cycle stage. Life cycle stage Eggs Fry e emergence to lake entry Fry e lake entry to first winter Fry e first winter Fry e smolt Post smolts Immature sockeye in ocean Returning adults Means for all life cycle stages Mean vulnerability scores for each region and temperature increase Upper e 2 C Upper e 4 C Mid e 2 C Mid e 4 C Lower e 2 C Lower e 4 C 3.17 2.42 2.42 2.36 2.45 2.46 3.04 3.69 2.75 4.21 3.54 3.75 3.18 3.27 3.46 3.96 4.58 3.74 3.17 2.67 2.67 2.27 2.55 2.63 2.96 3.35 2.78 4.13 3.79 3.75 3.18 3.36 3.63 3.88 4.27 3.75 3.25 2.67 2.42 1.91 2.36 3.04 2.95 3.12 2.71 4.13 3.71 3.67 2.55 3.09 3.79 3.95 3.92 3.60 Means for all regions and temperatures 3.67 3.13 3.11 2.58 2.85 3.17 3.46 3.82 Author's personal copy 2778 T. McDaniels et al. / Journal of Environmental Management 91 (2010) 2771e2780 Table 4 Mean overall vulnerability (on a scale of 1e5) of upper, mid, and lower sockeye salmon stocks at different temperatures. Temperature Overall vulnerability mean Upper fraser spawning grounds Mid fraser spawning grounds Lower fraser spawning grounds 2 C 3.58 2 C 3.42 2 C 3.27 4 C 4.73 4 C 4.50 4 C 4.19 Table 5 Mean ratings of own knowledge and confidence regarding sockeye vulnerability issues, by life cycle stage and overall. Life cycle stage Mean knowledge rating Mean confidence rating Eggs Fry e emergence to lake entry Fry e lake entry to first winter Fry e first winter Fry e smolt Post smolts Immature sockeye in ocean Returning adults Means for all life cycle stages As reported overall 2.54 2.54 2.62 2.46 2.54 2.46 2.69 3.62 2.68 3.13 2.54 2.42 2.42 2.17 2.42 2.29 2.54 3.23 2.50 2.42 The vulnerability of Fraser River sockeye to climate change increases from the lower to the upper Fraser River spawning regions, but the differences in vulnerability between regions was statistically significant only for the upper Fraser compared to the lower Fraser at 4 C. The difference between the 2 and 4 C temperature scenarios within each region was statistically significant (p < 0.01) for all regions. 4.4. Uncertainty Participants rated their overall knowledge of the workshop topics and confidence regarding workbook responses on a scale of 1e5 (5 being highly knowledgeable or confident and 1 not confident). The mean knowledge rating was 3.13 and mean confidence was 2.42, suggesting the participants did not have high confidence in either their knowledge or their judgments. This is despite the fact that the participants were among the best-informed technical and management specialists in the world regarding these fish resources. Participants were roughly equally uncertain about their judgments regarding each life stage except for returning adults, where they felt more knowledgeable and confident. Differences between the knowledge ratings for the returning adult stage and every other stage were statistically significant (p < 0.01) and differences in confidence between the returning adult stage and others were statistically significant (p < 0.05 for immature sockeye in ocean and eggs; p < 0.01 for the other life cycle stages). Note that participants’ self-assessment of their overall knowledge was higher than the mean of reported knowledge over all life cycle stages. Table 5 shows participants’ knowledge and confidence ratings for each life cycle stage. 4.5. Mitigation The second major task was to elicit the participants’ views regarding the potential to mitigate adverse effects of climate change on reproductive capacity of Fraser River sockeye salmon. We addressed two broad questions in a facilitated discussion: (i) what options are available to mitigate the effects of climate change on Fraser River sockeye stocks, and (ii) how practical are these options? The discussion began with the adult stage of the salmon life cycle, as participants explained that the ability of adults to reach spawning grounds was crucial to every other stage. Each life cycle stage was then examined in reverse sequential order. Participants were asked to discuss two kinds of options: (i) mitigation measures that involve changes in how fisheries are managed, and (ii) mitigation measures that involve the use of infrastructure of some kind. Table 6 summarizes the results. In general terms, the kinds of policy measures that could be pursued for returning adults are similar to those now being considered or implemented by fisheries managers in the Department of Fisheries and Oceans. Policy measures for other life cycle stages are unclear, except for perhaps predator management for the stage from lake entry to smolts. The only infrastructure measures that were viewed as practical were construction of additional spawning channels to aid returning adults and eggs. Investments in temperature management and flow augmentation were suggested as prospects in systems without lake influence. Importantly, temperature management in the mainstem of the Fraser River through construction of low level outlets on the Table 6 Climate change mitigation options for Fraser River sockeye. Life cycle stage Returning adults Immatures in ocean Post smolts, estuary, and coastal Fry: lake entry to Smolts Eggs Policy measures to assist with mitigation Adopt a balanced “fish friendly” approach that fostered adaptive management and policy coordination across species. Alternative fishing strategies to achieve escapement goals (thereby conserving genetic diversity) including: quota management, limited harvest and removal rates, more efficient fishing strategies,and an increased number of smaller fisheries. Not clear. At this stage the fish are widely dispersed and not necessarily \within Canadian jurisdiction. None suggested Participants argued for a multi-species monitoring program that could help identify predators early on, before they became established in a new ecosystem. Predator management to stop the spread and distribution of predators (e.g., preventing fishermen from moving bass from lake to lake or preventing the natural migration of predators). None suggested Infrastructure to assist with mitigation Create additional spawning channels, Cold-water release (to lower the temperature of the Fraser main stem or spawning streams) is not a viable option, given the volumes of water that would be required. None suggested Measures to aid in recovery of estuary ecosystems None suggested Constructing spawning channels and off-channel spawning places can best assist eggs. Investments in temperature and flow management should be made in systems without lake influence. Author's personal copy T. McDaniels et al. / Journal of Environmental Management 91 (2010) 2771e2780 existing Kenny Dam, or construction of dams on other tributaries were viewed as impractical and likely ineffective, given the volumes of water needed to alter temperature regimes in the mainstem of the Fraser River system. In sum, there are relatively few alternatives available to mitigate the effects of climate change on sockeye salmon in the Fraser River system. These fisheries are already tightly managed and nearly fully committed to various user groups. There are few or no new structural alternatives and little in terms of new management directions that could help mitigate the vulnerability of Fraser River sockeye to climate change. On the other hand, Fraser River sockeye already demonstrate a great deal of adaptive capacity in utilizing heterogeneous habitats in different river basins. Hence, this adaptability points to the potential value of policies that seek to make stocks more resilient to uncertain futures. Some authors have discussed the potential for future adaptation of salmon to climate changes (Crozier et al., 2008). Healey (2009) considers the resilience attributes of salmon and measures to enhance them. 5. Conclusions Participants clearly thought that sockeye salmon in the Fraser River system are vulnerable to climate change to the extent that reproductive capacity could be substantially impaired. This was particularly true for climate scenarios that predict greater temperature increase and for stocks spawning in the upper Fraser River system. Participants believed that returning adults and eggs were the life stages most vulnerable to climate change. The returning adults life stage was rated as the most vulnerable, and was also the life stage for which the participants had the highest knowledge and confidence ratings. Overall, participants stressed the many uncertainties regarding vulnerability estimates and the difficulty of predicting specific levels of impact. Finally, sockeye in the Fraser River system are highly adapted to specialized habitat conditions, which differ greatly from one river system to the next. Hence it is possible that the adaptive capacity they have demonstrated in the past may lead to spontaneous adaptation of warmer conditions through behaviour changes. For example, delayed run timing for stocks spawning in the upper portion of the system have been recorded in recent years. Mitigation of the impacts of climate change on sockeye salmon may be difficult because the resource management systems are already highly constrained, with overlapping demands on the resource from multiple gear types and sequential fisheries. Participants believed that efforts should be concentrated on fostering resiliency to climate change impacts instead of predicting specific levels of change. To facilitate adaptation, participants suggested improved information collection and strategic science-based learning to improve understanding of current system functions. This new information could help experts develop robust policies that are better able to cope with the irreducible uncertainties of climate change. Turning to the process developed and applied here, this is to our knowledge the first use of a structured process to elicit expert judgments of vulnerability to climate change for a specific species, in a specific habitat system, over its life cycle, differentiating among sub-groups. Ecological vulnerability to climate change has largely been addressed over large geographic areas (e.g., such as the Pacific Northwest states, as in Miles et al., 2007) or over many species (e.g., Walther et al., 2002; Parmesan and Yohe, 2003). These assessments have largely considered impacts of climate change to the present, without considering vulnerability of specific species to future change in particular locations. Here we used approaches informed by methods of probability elicitation (Morgan and Henrion, 1990), 2779 but within a more direct and less complex judgment task, to obtain judgments of vulnerability that integrate over many variables and scenarios. We sought the individual judgments of each participant, rather than attempting to create a consensus within the elicitation process, because of the importance of understanding the range of views (Morgan and Henrion, 1990). Based on this experience, the method appears promising for similar judgment tasks regarding vulnerability and climate change. The method could benefit from further applications and critical examination, as well as experimental testing of the kind that is sometimes employed for probability assessment. Any experimental tests would, however, face methodological hurdles similar to that arising for probability elicitation, such as the difficulty of judging calibration without rapid feedback on the results (Clemen and Winkler, 1999). Some might wonder whether the role of eliciting scientific judgments is as a contribution to science or more policy-relevant research. We do not claim that eliciting judgments creates new scientific knowledge. We do believe that synthesis of viewpoints regarding vulnerability of an ecologically-important species to climate change, based on existing scientific knowledge and the informed judgments of recognized experts, is an important contribution, as both meta-science and as a contribution to policy. Indeed, the whole IPCC enterprise addresses such a meta-analysis, but with a different method. The approach adopted here is a step toward more focused science that addresses key issues, such as the linkages among vulnerability among life stages of sockeye. But no matter how much research is devoted to these issues, the vulnerabilities summarized here will remain significant but uncertain threats to Fraser River sockeye salmon. Acknowledgements This research was made possible through support from the Climate Decision Making Center (CDMC) located in the Department of Engineering and Public Policy. This Center has been created through a cooperative agreement between the National Science Foundation (SES-0345798) and Carnegie Mellon University. The CDMC provided a sub-grant to the University of British Columbia for these efforts. The contributions by M. Healey were supported by an NSERC Discovery grant. We thank the expert participants who spent time working with us to provide their judgments and insights for this research project. References Burgner, R.L., 1991. Life history of sockeye salmon (Oncorhynchus nerka). In: Groot, C., Margolis, L. (Eds.), Pacific Salmon Life Histories. UBC Press, Vancouver, pp. 1e117. 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