Review of the Effectiveness of Recovery Measures for Southern Resident Killer Whales

Effectiveness of Recovery Measures

Table of Contents

• Complete Text
• 1.0 Context/Background
• 2.0 Objectives of this Review
• 3.0 Sources of Information
• 4.0 Methods for Assessing Effectiveness of Recovery Measures
• 5.0 Review of Recovery Measures
  • 5.1 Identified Threats and Broad Strategies
  • 5.2 A Review of Recovery Measures
• 6.0 Effectiveness of Recovery Measures
  • 6.1 Prey Availability
  • 6.2 Acoustic and physical disturbance
  • 6.3 Environmental Contaminants
  • 6.4 Ship Strike
• 7.0 Effectiveness of Recovery Measures related to Critical Habitat
• 8.0 Recommendations about priority of Recovery Measures
• 9.0 Conclusions
• 10.0 Acknowledgements
• 11.0 References
• Appendix 1

6.0 Effectiveness of Recovery Measures

The following sections identify the primary threats to SRKW recovery, characterize the threats, and review the efficacy of measures undertaken to date aimed at mitigating the threats. It is evident from Table 2 that many Recovery Measures (32) involve research aimed at improving the understanding of how a particular threat affects this population. Although these Recovery Measures do not directly result in threat reduction, knowledge and understanding gained from research is often necessary to guide and inform the management options that can lead to the mitigation of threats.

6.1 Prey Availability

Characterization of the threat

SRKWs are highly specialized predators and prey primarily on Chinook salmon. This selectivity is particularly evident during the months of May through September in the Salish Sea, when they forage almost exclusively on Chinook salmon in Juan de Fuca Strait, Puget Sound, the southern Strait of Georgia and off southwest Vancouver Island (Ford et al. 1998; Ford and Ellis 2005, 2006; Ford et al. 2010b; Hanson et al. 2010b; M. Ford et al. 2016; J. Ford et al. In Press). During October and November, SRKWs increase their use of Puget Sound, and are likely to feed on migrating Chum salmon as well as Chinook (Osborne 1999). By December, most of the SRKW community have left their summer core areas in the Salish Sea. In particular K and L pods are mostly absent from December to May. Although much less is known of SRKW diet in winter and early spring, sightings and acoustic recordings indicate that they range widely along the mainland US coast and off the west coast of Vancouver Island (Wiles 2004; Zamon et al. 2007 Hanson et al. 2013; Ford et al. in press). Their occurrence off the mouth of the Columbia River and in Monterey Bay, California, appears to be associated with local concentrations of Chinook salmon (Wiles 2004; Zamon et al. 2007; Hanson et al. 2010b).

The survival and recovery of SRKW appears to be strongly linked to Chinook abundance. Ford et al. (2010b) showed that mortality rates of both SRKWs and NRKWs were negatively correlated with Chinook salmon abundance over a 25-year period, from 1979-2003. In particular, a sharp decline in Chinook salmon abundance that persisted for four years during the late 1990s was associated with mortality rates up to 2-3 times greater than expected and resulted in population declines in both Resident Killer Whale populations. Ward et al. (2009) demonstrated a significant association between Chinook salmon abundance and reproductive rates in the SRKW population.

Due to their relatively large size and high lipid content, Chinook salmon are highly profitable prey for SRKWs and provide a high caloric gain for the energy expenditure of foraging (Ford and Ellis 2005, 2006). They have also been, at least historically, a reliable prey source. Unlike many species of salmon that spend large portions of their lifecycle on the high seas only returning to coastal waters to spawn, Chinook are available year-round in coastal waters. Killer Whales appear to preferentially select four to five-year-old Chinook salmon, which have mean body masses of 8-13 kg (Ford and Ellis 2005). These Chinook are considerably larger than mature Chum salmon (4.0-5.5 kg), which become more prominent in the diet in the fall, and are more than double the size of a typical coho or pink salmon, which they seldom eat (Ford et al. 1998).

Chinook abundance

The abundance of Chinook salmon in both Canada (British Columbia) and the US (Washington, Oregon and California) has been greatly reduced from historic levels and many populations are in decline. As a consequence many stocks, including 10 of 17 Chinook stocks in Washington, Oregon and California, are listed as threatened or endangered under the US Endangered Species Act (ESA) (NWR 2004), or identified as stocks of conservation concern in Canada. Chinook abundance in B.C. dropped in the 1970s and 1980s, but escapements (number of fish entering the river to migrate to spawning areas) increased until the early 1990s in some rivers. This increase is primarily due to hatchery production and reduced harvest rates following implementation of the Pacific Salmon Treaty in 1985 (Beamish et al. 1997). However, several of those stocks have again decreased substantially in abundance over the last three generations (Riddell et al. 2013). Recently, seven Fraser River Chinook conservation units (CU) were designated as red (highest level of concern) and two others as amber (lower level of concern) in a process that applied the Wild Salmon Policy status categories based on various measures and indicators of status (DFO 2016b; Grant and Pestal 2013). Although there are 15 CUs recognized in the Fraser River system, only eleven had sufficient data for evaluation. The last 12 to 15 years have been a period during which most groups of Chinook within the Fraser River have declined in numbers, and the outlook for Chinook outside of the Fraser River has generally not shown sustained improvement since 1990 (DFO 2016b).

In Washington, hatchery fish now account for about 75% of all harvested Chinook, which is a concern for genetic diversity and productivity of Chinook populations (Mahnken et al. 1998 in Wiles 2004). Declines in abundance of spring-run Chinook salmon have been particularly evident in California's Central Valley, in the Columbia River (interior spring Chinook salmon), and in Puget Sound. Associated with the declines in abundance, there have also been shifts in age structure of many populations toward younger ages and smaller adults. In addition to reduced Chinook abundance, the size and thus nutritional value of individual fish appears to have declined over recent decades. Between 1975 and 1993, up to a 45% decline in the average mass of Chinook salmon was observed in nine populations from British Columbia to California (Bigler et al. 1996). Thus, the nutritional yield of each Chinook salmon is significantly less today than it was in past years and negatively impacting the overall foraging energetics of SRKW (Krahn et al. 2004, 2002).

Genetic identification of prey samples indicates that SRKW foraging in the Salish Sea and off the west coast of Vancouver Island are feeding primarily on Fraser River system Chinook, but also some Puget Sound and southeast Vancouver Island stocks (Ford et al. 2010b; Hanson et al. 2010b). The Fraser River system contains the largest spawning populations of Chinook on the west coast of North America. Diet studies of SRKW indicate that Chinook from different stocks appear in the diet roughly in proportion to their relative abundance (Ford et al. 2010b; Ford et al. In Press; Hanson et al. 2010b).

A 2013, photogrammetry study assessed SRKW body condition in 43 SRKWs and demonstrated a decline in body condition of 11 animals including 7 prime-age females compared to their condition in 2008 when 43 animals were also assessed. In the 2013 study, twelve SRKWs were identified as pregnant, based on breadth measurements from these aerial photos. However, only two of these animals were subsequently seen with a calf, suggesting that poor body condition is a likely factor (Fearnbach et al 2015).

In 2017, a review of recent research on SRKW was undertaken to detect evidence of poor body condition in the population (Matkin et al. 2017). This review examined evidence from sightings data (photo-identification and mortality), aerial photogrammetry, necropsy data, and fecal hormone analyses. The independent science panel that conducted the review concluded that there were multiple lines of evidence that indicated the presence of poor body condition in SRKW, and that this was associated with loss of fetuses, calves and adults.

Recovery Measures to address this threat

Chinook abundance In 2011 and 2012, DFO collaborated with the National Oceanic and Atmospheric Administration (NOAA) in a series of three scientific workshops that rigorously reviewed the available information on SRKW, their feeding habits, and the potential effects of salmon fisheries on SRKW through reductions in prey abundance. A panel of independent scientists was selected to oversee and participate in the process and produce a report documenting its findings (Hilborn et al. 2012). The report acknowledged the large body of scientific research on population effects of reduced prey availability, but concluded that caution was warranted in assigning a causative relationship to the correlation between the coast wide Chinook salmon abundance index and SRKW survival. In addition, the panel noted that reductions in coast-wide Chinook harvest would not necessarily lead directly to a greater availability for SRKWs. This was based on the reliance of SRKWs on Fraser River stocks and some Puget Sound stocks of Chinook salmon such that a coast wide closure of Chinook salmon fisheries (which is a mixed stock fishery) would not necessarily lead to direct increases in Chinook salmon from these stocks becoming available to SRKWs. They also noted that increases in abundance in Chinook salmon that may result from coast wide closures could be negated by competition from Northern Resident Killer Whales, seals and sea lions.

Hilborn et al. (2012) provided a series of recommendations for future work which were included as Recovery Measures in the Action Plan. Their recommendations emphasised the value of ongoing assessments of body condition as an indicator of reduced prey availability as well as a need for greater effort to identify their winter diet (Hilborn et al. 2012).

In 2005, DFO introduced the Wild Salmon Policy (WSP) to guide conservation and management of Pacific salmon species. The WSP set out an approach involving the identification and assessment of the biological status of conservation units of Chinook salmon. The conservation units were ranked according to their biological status and the rankings were used to target subsequent research and management actions. For, example, numerous Chinook conservation units from the Fraser River system, as well as many others in southern BC, were assessed with biological status in the "red zone" indicating a high level of concern, and triggering a requirement under the WSP for "immediate consideration for ways to protect fish, increase abundance and reduce the risk of loss" (DFO 2016b).

Chinook salmon stocks in southern BC are caught not only in coastal BC fisheries but also in Washington State and Alaska fisheries. The Pacific Salmon Treaty (PST) commits Canada and the U.S. to carry out fisheries and enhancement programs and includes provision for bilateral cooperation to limit harvest that would be beneficial for conservation of important stocks. Compared with the 1990 PST, its renewal in 2009 included a 15% reduction in the harvest of Chinook salmon in the Southeast Alaska (SEAK), and a 30% reduction in the west coast of Vancouver Island (WCVI) aggregate abundance based management (AABM) Chinook fisheries. As part of the 10 year renegotiation cycle, the current provisions of the Chinook salmon fishery chapter are being renegotiated by the two countries and continuation of the existing fishery reductions and other adjustments are a key area of discussion. The Pacific Salmon Commission's (PSC) Chinook Technical Committee, which evaluates the management regime, has noted deficiencies in data on numerous stocks that have impacted evaluations of the effectiveness of the management regime (PSC 2016). While these management actions and the development and implementation of the WSP are underway, it is not clear whether they have resulted in a positive effect for SRKWs. However, it is worth considering that the availability of prey for SRKWs could be an even greater threat were these actions and efforts not in place.

DFO has compiled two data reports to support the current COSEWIC assessment of southern BC Chinook salmon. In addition, in 2012, DFO entered into a bilateral planning process with First Nations and other collaborators called the Southern BC Chinook Strategic Planning Initiative. The overall goal of this initiative is to develop a strategic plan that will address the challenges facing these stocks, such as depressed and/or declining spawner abundance, reduced and variable freshwater and marine survival rates, pressures on freshwater habitat, total mortalities associated with harvest, increased predation, and ecosystem effects from climate changes. The draft strategic plan includes six biological objectives, one of which is particularly relevant to SRKWs and offers considerable potential to ensure prey availability for this population. Specifically, under the objective: "Sustain salmon contribution to ecosystem health", there are two specific sub-objectives: 1) ensure that there are sufficient Chinook salmon post-harvest to sustain Chinook-dependent predators and 2) ensure that Chinook salmon harvests are not harming Resident Killer Whale populations. The indicator and performance measures listed are: 1) sensitivity of fecundity and population growth rate of SRKWs to current harvest rates of Chinook salmon; and 2) changes in the relationship between SRKW metrics and Chinook salmon abundance indicators. While the document is still in draft, the inclusion of these objectives, indicators and performance measures demonstrates a consideration of the relationship between Chinook salmon abundance and Recovery Measures for SRKWs (Table 2).

Only two of the 98 Recovery Measures in the Action Plan (#28 and 29) are specifically directed to the recovery of Chinook salmon stocks in Canada. There are a number of efforts underway that align with these measures (Table 2). There are at least four additional Recovery Measures (#3, 9, 25, and 26) that relate to research that could support implementation of improved fisheries management actions (Table 2). Implementation of these latter measures has been initiated or is ongoing and requires strong collaboration between personnel conducting salmon stock assessment and marine mammal researchers to ensure needed information is available for incorporation.

Chinook Availability. Initial efforts to address the threat of reduced prey availability focused on demonstrating a causal relationship between the coast-wide Chinook abundance index and SRKW mortality, with the intent of informing Chinook management actions. As discussed above, there is limited evidence to suggest a coast wide closure of the Chinook salmon fishery would address the issue of prey abundance for SRKWs; however more targeted reductions in Chinook salmon harvest will likely be beneficial and measures to address the threat of reduced prey availability in key foraging areas are currently being investigated.

There are a number of activities that have been recently implemented in DFO that have potential to deliver measurable outcomes for Recovery Measures # 6, 7, 8, 10, 27 which relate to the consideration of SRKW prey requirements in fisheries management decisions. Identification of SRKW foraging areas has already been completed, and pressures from fishing activities in these areas is under assessment. Assessment results will provide managers with the opportunity to consider strategic salmon fishery planning approaches and management actions that have the greatest likelihood of increasing the availability of Chinook salmon for SRKW in the locations and at the times that foraging is most likely to occur. Considerations such as reductions in Chinook salmon removals through fishery area boundary adjustments or closures, or changes to retention limits will be focused on foraging grounds, and subsequent evaluation of the effectiveness of these management measures will be implemented.

In support of these measures, information about SRKWs, their reliance on Chinook salmon, and the threats to their survival were included in the Integrated Fisheries Management Plan for 2016/17 (IFMP 2016). As such, this IFMP which sets out the management plans for salmon fisheries in B.C. represents an important step towards incorporating consideration of SRKW needs in Chinook salmon fisheries management (Table 2), although it does not propose specific fishery management actions

Effectiveness of Actions

Much of the research described above related to characterization of the importance of Chinook salmon availability to SRKW has occurred since 2003. Results to date confirm this species as the dominant prey for at least half of the year, and demonstrate a correlation between SRKW health and prey availability and have prompted an evaluation of management options to support recovery. Research on these topics is ongoing (and captured in one of 13 Recovery Measures in Table 2 and as new findings emerge they will continue to inform and guide management-based Recovery Measures.

Management measures taken by DFO to reduce harvest pressure on Chinook salmon on the B.C. south coast aimed at conserving key Fraser River Chinook stocks should be of benefit to SRKWs. There is, however, little evidence that management actions that would directly support Chinook salmon availability for SRKWs in key foraging locations have been implemented. The NOAA-led transboundary workshop (Hilborn et al. 2012) as well as several CSAS research documents that assess the Chinook salmon needs of SRKWs (e.g. Ford et al. 2010b; Vélez-Espino et al. 2014a; 2014b) aim to inform management actions, but to date, have not led to specific fishery management actions. However, the recent shift in approach from focusing on Chinook abundance, to supporting Chinook availability in SRKW foraging grounds has led to the initiation of science-based advice in support of strategic salmon fishery approaches and management actions to reduce the competition SRKWs experience from Chinook fishing. In addition, the inclusion of objectives regarding SRKW's prey requirements in the Integrated Strategic Plan for Southern BC Chinook, and the description of their needs in the salmon IFMP represents some progress.

6.2 Acoustic and physical disturbance

Characterization of the threat

Acoustic disturbance and physical disturbance are considered together here because it is often not clear whether it is physical presence (e.g., boats getting in the way of whales) or acoustic impacts (underwater noise created by vessels or other anthropogenic activities that mask communication and echolocation signalling) together or separately that are negatively affecting whales.

Killer whales use sound for communication, prey detection, and to acquire information about their environment. These animals produce a variety of sounds including echolocation clicks for foraging and navigation and pulsed calls and whistles during social interactions. Call production is believed to serve important roles in the social dynamics of groups that travel and forage together (Ford 1989). Resident killer whales appear to make extensive use of echolocation to locate and capture prey, though vision may also play a role at close ranges (Ford 1989; Barrett-Lennard et al. 1996). Studies of echolocation click structure and the sound energy content of the clicks in NRKWs suggest that they should be able to detect Chinook salmon at ranges of about 100 m in average conditions, and less so as ambient underwater noise increases (Au et al. 2004).

It is estimated that ambient (background) underwater noise levels have increased an average of 15 dB (note a 3dB increase represents a doubling of noise levels) in the past 50 years throughout the world's oceans (NRC 2003). Shipping noise is the dominant source of ambient noise between 10 to 200 Hz but, ships also produce significant amounts of higher frequency noise in the audible range (600Hz to 114kHZ with the greatest sensitivity in the range of 5kHz to 81kHz, Branstetter et al. 2017) of killer whales. Noise received from ships at ranges less than 3 km in the relatively narrow passage of Haro Strait, an area frequented by SRKWs, extend upward into frequencies used by SRKWs (Veirs et al. 2015).  It is widely recognized that commercial shipping has increased dramatically in recent years. Currently in the Salish Sea one large ship transits the area, on average, every hour of every day of every year, with three transits per hour observed at the busiest times (Erbe et al. 2012 Williams et al. 2014a). Within the Salish Sea, commercial shipping is the dominant source of overall sound energy, but smaller craft (recreational, fishing, whale watching boats) are a substantive contribution in certain sub-areas of the Salish Sea (ECHO 2016). In Puget Sound one year of ship traffic data was paired with hydrophone recordings to assess ambient noise and quantify contribution of vessel traffic. Commercial vessel traffic accounted for more than 90% of the sound energy budget, with container ships as the greatest contributor (Bassett et al. 2012).

Whale watching and recreational boating activity has also increased as a result of increasing interest in ecotourism, and a growing human population around the Salish Sea. Commercial whale watching in the Canadian and U.S. portions of the Salish Sea increased from a few boats in the 1970s to about 80 boats in 2003 and in 2016 to 100 boats; this estimate does not include the recreational boaters (Holt 2017). Non–commercial boats include kayaks, sailboats and powerboats. Whale watching activities have the potential to disturb marine mammals through both the physical presence and activity of all types of watercraft, as well as the increased underwater noise levels that boat engines generate (DFO 2011).

Trends in acute noise from such activities as dredging, drilling, or blasting in SRKW habitat are not reviewed here due to the time frame available to complete this review.

Anthropogenic noise, either chronic (e.g. shipping noise) or acute (e.g. pile driving, blasting, seismic surveys and other types of hydro-acoustic related surveying and navigation), can interfere with the ability of SRKWs to conduct their life processes. Such disruptions are associated with decreased foraging success, displacement of animals from preferred feeding habitats, displacement of prey, impaired hearing, either temporarily or permanently (Barrett-Lennard et al. 1996; Erbe 2002, Bain 2002, NRC 2003, Au et al. 2004).

Studying the effects of noise on cetaceans involves complex modelling of sound propagation and information on the auditory hearing sensitivity of a species. Erbe (2002) modelled the noise of whale-oriented boat traffic in the vicinity of SRKWs and showed that the noise of fast boats could mask their calls within 14 km, could elicit a behavioural response within 200 m, and could cause a temporary threshold shift (TTS) in hearing of 5 dB after 30–50 min within 450 m. Boat speed was a significant factor in determining the amount of noise generated. Slowing speed, which results in less noise, masked signals at 1km from the boat. However, there are typically many boats in the vicinity of SRKWs, so modelled noise levels associated with a number of boats around the whales were found to be close to the critical noise threshold assumed to cause a permanent hearing loss over prolonged exposure.

Numerous studies since 2002 have demonstrated behavioural response and changes in acoustic signalling by SRKWs living and foraging in the Salish Sea that strongly suggest an energetic cost and potential stress to SRKWs associated with the increased noise levels. Specifically, SRKWs significantly increased the duration of their calls when boats were present and increased the amplitude of their calls as background noise level increased as a result of the number of vessels nearby (Foote et al. 2004; Holt et al. 2009; 2011).

SRKWs were observed to be within 400 m of a vessel most of the time during daylight hours from May through September, largely as a result of whale-watching oriented vessels approaching and following them. Studies of SRKW behaviour in the vicinity of whale-watching oriented vessels in the Salish Sea showed that SRKWs were significantly less likely to be foraging and significantly more likely to be traveling when boats were around and were displaced short distances by the presence of vessels (Lusseau et al. 2009). Behavioural responses to close approaches of boats include an increase in surface active behaviour which may have increased energetic costs (Noren et al. 2009).

The response of SRKWs to vessels is likely a result of acoustic disturbance and in the case of small vessels that may approach them, due to physical disturbance as well. Williams et al. (2014b) estimate that in the noisiest sites in Canadian Pacific waters, SRKWs will lose up to 97% of their acoustic communication space in the frequencies used for social communication calls.

A Killer Whale-Noise-Exposure simulation model based on sound propagation modelling, a behavioural dose response model (SMRU Consulting Canada 2014), and published audiograms of killer whales indicate that noise from vessels regionally in the Canadian portion of the Salish Sea is likely impacting SRKW's ability to forage successfully. Time lost from foraging across all vessels types is estimated at 20-23% of each whale day. Two-thirds of this lost time is considered to be due to behavioural responses which are caused predominantly by large ships (generally vessels of 500 tons or more), although whale watching boats (small vessels) are predominantly responsible for the remaining high sound frequency click masking noise (RBT2 2013).

Recovery Measures to address this threat

There are at least 12 Recovery Measures in the Action Plan that are relatively immediate actions aimed at mitigating noise levels in the Salish Sea, assessing cumulative effects of development projects and other human activities, and reducing noise and disturbance from largely whale-watching oriented boat traffic through education, enforcement and whale watching guidelines (Table 2; e.g. Recovery Measures # 12, 31, 34, 35, 41, 10, 11, 13, 47, 49, 50, and 53).

Among these there are six Recovery Measures (# 31, 34, 47, 49, 48, 43) aimed at addressing the problem of increasing ambient noise from shipping in the Salish Sea which have had some recent achievements. In 2012 the World Wildlife Fund organized a workshop to further the understanding and management of ocean noise on the Pacific coast. The workshop identified actions including establishing baseline ocean noise levels and scenarios of possible change, integrating hydrophone networks and informing placement for further hydrophones, and providing policy recommendations for noise mitigation (Heise and Alidina 2012). Since then, DFO undertook a coast-wide inventory of hydrophone installations as a first step to developing a network of calibrated hydrophones in Canadian waters. This is an identified Recovery Measure.

Analysis of acoustic data from the Canadian portion of the Salish Sea has been undertaken to determine the vessel sectors that contribute different levels of noise in the various sub-regions. The purpose of this on-going effort is to identify sub-regions where noise mitigation is needed for SRKWs to guide mitigation efforts (ECHO 2016).

The Vancouver Fraser Port Authority has led an initiative aimed at better understanding and managing the impact of shipping activities on at-risk whales, in particular SRKWs throughout the southern coast of British Columbia. The initiative is called Enhancing Cetacean Habitat and Observation (ECHO). The long term goal of the ECHO Program is to develop mitigation measures that will lead to a quantifiable reduction in potential threats to whales as a result of shipping activities. Approaches include identifying vessel noise source levels and developing mitigation measures such as voluntary slow zones, hull cleaning or incentives to adopt quietening technology (e.g. reduced port fees) (Port Vancouver 2017). To guide the program, there are advisory groups and technical working groups that include DFO membership.

The Vancouver Fraser Port Authority also established a Technical Advisory Group (TAG) to enhance the relevance, quality, and rigour of the Environmental Assessment studies that would be needed for the Roberts Bank Terminal 2 proposed development. The focus of the TAG was on SRKWs. The work of the TAG led, in part, to the estimate of lost foraging time and a SRKW dose response curve for behavioural effects to noise (SMRU Consulting Canada 2014; ECHO 2016; RBT2 2013).

DFO maintains a 24-hour hotline (BCMMRN/ORR) to report incidents involving whales. NOAA has a similar system as well as on-line reporting. In Canada, promotion of whale watching guidelines, on-the-water voluntary compliance programs, and enforcement efforts are underway. There have been four successful prosecutions of individuals for causing disturbance to resident killer whales in Canada since 2003. In the US, whale watching regulations are also enforced. Regulations implemented in 2011 in Washington State prohibit vessels from approaching within 200 yards of killer whales and from positioning within 400 yards of the path of killer whales. In Canada the Be Whale Wise Guidelines ask that people operating vessels stay 100m away from whales and slow their speeds within 400m of whales, travel parallel to them, and avoid approaching within 400m of the path of the whales. New regulations that would enforce these guidelines in Canada under the Fisheries Act are in development.

Effectiveness of actions

The research referenced in the characterization of the threat section above has largely occurred since 2003. Although the state of knowledge in 2003 included some behavioural studies on Northern Resident Killer Whales (Williams et al. 2002a; 2002b) and acoustic modelling (Erbe 2002), it is clear that the research since then has led to a demonstrably better understanding of this threat, which will continue to inform and guide management-based Recovery Measures.

Recovery Measures that aim to modify the behaviour of recreational and whale watching vessels through voluntary restrictions and disturbance charges leading to conviction (Canada), regulated restrictions about minimum whale watching viewing distances (U.S.), and education and outreach activities have increased in recent years. Collectively these implemented measures have likely had a positive effect on altering the behaviour of people in small boats on the water, thereby likely reducing acoustic and physical disturbance from small boats. However their collective effectiveness, in terms of measurable reductions in noise or disturbance is uncertain. Effectiveness could be inferred from an estimate of the number of boats within a certain distance of whales during summer annually, but this statistic was not found in time for this this review. Completion and formulation of Canada's Marine Mammal regulations under the Fisheries Act would make an enforceable contribution.

Underwater noise from vessels in the Salish Sea is high, but a quantitative time series was not available at the time of this review demonstrating an increase in underwater noise levels since 2003 or over a longer time period. However, it can be inferred that increases in whale watching boats, shipping traffic and further projected increases in shipping activity have led to increases in the underwater noise since 2003. Recovery actions aimed at mitigating noise in the Salish Sea from shipping have advanced significantly in recent times and were nonexistent in 2003. Collectively these activities, primarily since 2012, have further advanced the understanding of the threat. Efforts by the Vancouver Fraser Port Authority and their ECHO program have brought together expertise from different areas (DFO, academia, research and development companies, and shipping industry etc.; Table 2) to identify and refine mitigation options for reducing shipping noise in SRKW habitat. However no specific mitigation actions have been implemented yet.

6.3 Environmental Contaminants

Characterization of the threat

The threat of environmental contaminants encompasses chemical, particularly bio-accumulating chemical contaminants and biological pollutants. These later contaminants may be pathogens that enter SRKW habitat from coastal runoff and through wastewater from urban and agricultural areas and possibly through airborne transport. These two categories are discussed separately below. The Salish Sea is surrounded by increasing urban development and industrialization. There are local regional and global inputs of contamination. The issue is also made more complex because Canada and the U.S. have different regulations to address this transboundary threat and an effective solution will require greater collaboration and harmonization.

Chemical contamination

Killer whales are vulnerable to accumulating high concentrations of Persistent Organic Pollutants (POPs) because they are long-lived animals that feed high in the food chain (Ross et al. 2000, 2002, Rayne et al. 2004; Ross 2006). POPs are persistent, they bio-accumulate in fatty tissues, and are toxic. Resident killer whale prey, primarily Chinook salmon, feed in the upper trophic levels in the food web too and several stocks of importance to SRWKs reside in Salish Sea and in other coastal marine areas for a considerable amount of their life cycle.

POPs include 'legacy' contaminants such as the polychlorinated biphenyls (PCBs), and the organochlorine pesticide DDT, which are no longer widely used in industrialized countries, but remain persistent in the environment. The so-called 'dirty dozen' POPs are encompassed under the terms of the Stockholm Convention which aims to phase out use of chemicals of global concern. Additional contaminants of 'current concern' include flame retardants such as polybrominated diphenylethers (PBDEs) as well as currently used pesticides.

PCBs

Mean total PCB concentrations in SRKW sampled 1993-96, greatly exceeded those measured in the highly contaminated St. Lawrence beluga whales, Delphinapterus leucas (Ross 2000). The PCB concentrations in SRKWs at that time were well above levels associated with toxic effects in harbour seals and indicate that SRKWs are at risk of adverse health effects including immunotoxicity, reproductive impairment and endocrine disruption (Ross et al. 1996). Total PCBs in SRKWs tissues in 2004 and 2006 appeared to have decreased from 1993-96 however the levels still exceeded the threshold associated with health effects in harbour seals (Krahn et al. 2007). Blubber biopsy samples from NRKW obtained in 2003 to 2007 were analyzed to consider the effects of PCBs on mRNA transcripts related to KW health and found PCB-related increases in the expression of five of these gene targets. These results indicate there are on-going adverse physiological effects of PCBs in NRKWs and thus this is undoubtedly true in SRKWs as well (Buckman et al. 2011).

PBDEs

Fire retardants (PBDEs) are a significant and emerging concern for SRKWs (Ross 2006). Three main types of PBDEs are used in consumer products: Penta-BDE, Octa-BDE and Deca-BDE. Moderate levels of total PBDEs were observed in 39 biopsy samples collected from SRKWs in the years 1993-1996. Concentrations in the environment increased exponentially in the 2000s. The endocrine-disrupting potential (negative effects on reproduction, early development etc.) of PBDEs has been established in laboratory animals, fish and in seals. PBDEs are being introduced to the marine environment by wastewater discharges and atmospheric deposition (Rayne et al. 2004; Ross et al. 2008; Ross et al. 2009).

Current and historical concentrations of PCBs and PBDEs were modeled in individual SRKWs. Total PCB concentrations were predicted not to increase significantly over time, but PBDEs were predicted to have increased with time and with age, with a doubling time of 3-4 years. J pod, which spends the most time in the Salish Sea was predicted to have the highest concentrations of both PCBs and PBDEs (Mongillo et al. 2012).

Chemical Contaminant levels in Chinook salmon

Unlike other salmon, many populations of Chinook salmon remain in nearshore waters during the ocean phase of their life cycle and they are relatively long-lived compared to other salmon species. As a result they are more vulnerable to pollution through prolonged exposure. Chinook salmon generally have higher concentrations of persistent bioaccumulating toxins than other Pacific salmon species (Mongillo et al. 2016).

For example, 97 to 99% of PCBs, polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), DDT, and hexachlorocyclohexane (HCH) in returning adult Chinook salmon in southern BC were acquired during their time at sea, which, in the case of ocean-type Chinook salmon includes coastal marine waters rather than high seas habitat. Highest POP concentrations (including PCBs, PCDDs, PCDFs, and DDT) and lowest lipids were observed in returning adult Chinook salmon sampled near the Lower Fraser River and in Puget Sound near rivers of destination. It is known that Chinook salmon experience migration-related loss of lipid content as they approach their natal rivers because they stop feeding during this time. The lower lipid content of Chinook salmon as they near their natal rivers in southern BC may cause SRKWs to increase their salmon consumption, relative to NRKWs by as much as 50% to obtain sufficient caloric value, thereby increasing their exposure to POPs (Cullon et al. 2009).

It has been suggested that exposure and accumulation of POPs may exacerbate mortality of SRKWs during periods of reduced Chinook salmon abundance resulting in nutritional shortages (Lundin et al. 2016). Under such conditions SRKWs would likely need to gain energy by mobilizing their fat stores (blubber) which would also release PCBs to be metabolized. This could lead to elevated liver enzymes that are related to deleterious effects on reproduction and immune function.

Recovery measures to address this threat

There are a number of Recovery Measures that could result in a relatively immediate reduction to the threat (e.g., Recovery Measures 73, 74, 79, 80). Some measures to address this threat have been initiated while others have not.

The Government of Canada has taken multiple actions to reduce the releases of some contaminants. Regulatory bans on certain chemicals, updates to regulations regarding disposal and new regulations for wastewater effluent have been put in place, some prior to 2003, others after 2003. These are discussed below and include activities that align with most of the listed Recovery Measures associated with this threat.

For example, DDT was widely restricted in both Canada and the U.S. in the 1970s and entirely banned from use by the 1980s. PCB production was banned in North America in the 1970s, although they are still used industrially and commercially in closed applications (e.g. in transformers and capacitors); however, this is tightly regulated throughout North America (Grant and Ross 2002).

The manufacture, use, and import of many contaminants of concern, including polybrominated diphenyl ethers (with the exemption of manufactured items), polybrominated biphenyls, perflurooctane sulfonate, short-chained chlorinated alkanes, tributyltins, polychlorinated naphthalines, and polychlorinated terphenyls are prohibited in Canada under the Prohibition of Certain Toxic Substances Regulations, 2012.

For dioxins and furans, polycyclic aromatic hydrocarbons, mercury, lead, cadmium, and copper, the Government of Canada has put in place a number of measures aimed at reducing emissions of these contaminants.

Regarding nonylphenol and its ethoxylates, the Government of Canada published a Pollution Prevention Planning Notice for textile mills and manufacturers and importers of cleaning products which resulted in a reduction of nonylphenol and its ethoxylates by 99.99% and 96% in these sectors, respectively.

Although some of these actions occurred well before 2003, given the persistent nature of many these substances, improvements will continue to occur with the passage of time.

Internationally the Government of Canada has been working with other countries to minimize exposure to contaminants from foreign sources. This includes work under the Stockholm Convention which aims to prohibit POPs, many of which are outlined in Appendix 2 of the Recovery Strategy (DFO 2011) and work under the Minimata Convention (Canada ratified in 2017) on mercury which aims to protect human health and the environment from the adverse effects of mercury. Canada ratified the Stockholm Convention in 2001; however, the work under the convention is ongoing to address Persistent Organic Pollutants.

Within Canada, Environment and Climate Change Canada (ECCC) and Health Canada (HC) are each responsible for evaluating regulatory performance to determine the efficacy of regulations. For example, under the Canadian Environmental Protection Act, 1999 (CEPA 1999), two to three million tonnes of material are disposed of at dedicated sites in the marine environment. The CEPA Action Level for disposal of potentially contaminated material at sea was found to be too high to protect killer whales due to the bio-accumulative nature of PCBs (Lachmuth et al. 2010). As a consequence in 2011-12, ECCC developed Standard Operating Procedures with DFO in order to address any additional risks associated with dredging/disposal in the Critical Habitat of resident killer whales. More restrictive PCB limits on sediment concentrations were subsequently introduced, based on modelling which took into account bioaccumulation (Alava et al. 2012). Because PCBs have largely been banned for the past 40 years, levels in sediment are slowly degrading or becoming buried by sediment deposition. Thus, the more restrictive limits as well as burying of contaminant sediment with cleaner sediment can serve to lower exposure to legacy sources of PCBs (Lachmuth et al. 2010).

Improvements to water quality protection were introduced in Canada in 2012 through the Wastewater System Effluent Regulations (WSER) (Government of Canada 2012). The WSER sets minimum regulatory effluent quality standards to be achieved through secondary wastewater treatment. The higher standard required will lead to removal of over 95% of the total mass of conventional pollutants in wastewater. Significant amounts of non-conventional pollutants and bacteria that may be present will also be removed through such treatment. The WSER sets out the timeline by which wastewater treatment facilities must meet the new standards. Wastewater systems considered of high risk to contaminate the environment are required to meet the effluent quality standards by the end of 2020, medium risk facilities by the end of 2030, and low risk facilities by the end of 2040.

Research to support the WSER included a study that analyzed PBDE congeners and levels in 20 wastewater treatment plants in Canada. The resulting profile of PBDE congeners in the influent provided a reference point for future PBDE monitoring in wastewater against which to evaluate the effectiveness of the 2012 regulation. The results of the study also provided operational recommendations to achieve higher percentages of PBDE removal from waste water (Kim et al. 2013).

DFO's National Contaminants Advisory Group has contracted for the following study which will provide key information on contaminant levels in SRKWs and health effects using genomic techniques:

Health risk-based evaluation of emerging pollutants in killer whales (Orcinus orca): priority-setting in support of recovery. Led by Frank Gobas and Peter Ross

In Washington State, the Department of Ecology undertook an assessment and identified the major sources of several chemical pollutants in Puget Sound, including PCBs, as a key step towards reduction of this threat (Ecology and King County 2011).

Washington's PBDE Law of 2008 (RCW 70.76) placed restrictions on the use of PBDEs in products sold in Washington. Manufacturers of Penta-BDE, Octa-BDE voluntarily ceased production beginning in 2004. Deca-BDE manufacturers agreed to discontinue the manufacture, import, and sales of Deca-BDE at the end of 2012. By 2013 USA companies were required to phase out the production and use of Deca-BDEs (USEPA, 2010a). Deca-BDE was banned in the US from televisions, computers, and residential upholstered furniture beginning January 1, 2011

A series of workshops hosted by NOAA and the EPA were conducted in 2013; topics included PBDE modeling in Puget Sound and the need to establish a PBDE toxicological threshold for SRKW. Knowledge gaps toward establishing this threshold were identified and recommendations were made for future research (Gockel and Mongillo 2013).

Effectiveness of actions

The actions presented above indicate collectively positive steps to abate the threat of at least some chemical contaminants in the marine environment and most of these actions align with many of the Recovery Measures associated with this threat. While the ban on DDTs and PCBs appears to have been similar in both countries and has been effective at reducing these contaminants in the environment generally, the restriction on PBDEs appears to differ between Canada and the U.S. Nonetheless, overall the regulations have probably reduced at least some PBDEs from accumulating in the marine environment. In 2008, Canada prohibited the manufacture (but not the use) of all PBDE congeners and also prohibited the use, sale, offer for sale, or import of certain PBDEs, as well as mixtures, polymers and resins containing them. In 2016, the prohibition on PBDEs was expanded to include the manufacture, use, sale, offer for sale, or import of all PBDEs and products containing PBDEs with an exemption for manufactured items. In contrast the US appears to have focussed on prohibiting the manufacture of three PBDE congeners and taken further steps to prohibit the use of one of these congeners, DECA-BDE by 2013.

PBDEs are thought to make their way into the marine environment primarily through wastewater and run off. In Puget Sound, for example, PBDEs are found in significant amounts in wastewater discharges (~ 25-38% of total PBDE loading into Puget Sound (Gockel and Mongillo 2013)). Although Canada has not prohibited all uses of PBDEs, its wastewater regulations set standards for wastewater quality that are required to be implemented by 2020 for high risk facilities, 2030 for medium risk facilities, and by 2040 for low risk facilities. As wastewater systems are upgraded to achieve these standards in the coming decades, reductions of PBDEs entering the marine environment are anticipated. However it is important to note that full compliance is not expected for over 20 years.

There are a number of Recovery Measures that would support reduction of chemical pollutants (e.g., Recovery Measures # 66, 68, 69, 70, 71, 75, 76, 77, 78, 97) but little appears to have been initiated in Canada (Table 2). In particular, there is, as yet, no oil spill response plan in Canada specifically for marine mammals including SRKWs or their habitat. However, adjacent, Washington State has developed and adopted such a plan. In the U.S. there have been some efforts to identify sources of POPs that are of concern for SRKWs and to try to develop toxicological thresholds for PBDE levels in SRKWs, (see Ecology and King County 2011 and Gockel and Mongillo 2013).

Ultimately a measure of effectiveness is reduction in the level of contaminants in marine food webs. SRKWs are long lived animals and thus declines in body burden of bioaccumulating POPs are not to be expected over a period of decades in the same cohort of animals. Hickie et al. (2007) modelled estimates of PCB concentrations in SRKW from 1930 to 2030 and estimated that the PCB concentrations in SRKWs would not fall below the threshold concentration associated with onset of toxic effects (17 mg/kg) in marine mammals until at least 2063. They concluded that despite adoption of regulations and source controls for PCBs in the 1970s these long-lived aquatic mammals are not protected by current Canadian or U.S. PCB dietary residue guidelines, because PCB concentrations in Chinook salmon would also have to drop. Contaminant levels, however, in shorter-lived top predators such as the harbour seal will reveal recent trends in contamination of the food chain. PCB concentrations in harbour seals, in the Salish Sea were found to have declined by 81% between 1984 and 2003, a not unexpected finding given the earlier ban on PCBs. Total PBDE concentrations which doubled every 3.1 years between 1984 and 2003, appeared to drop in 2009 possibly reflecting the withdrawal of the penta- and octa-BDEs from the market in the U.S. in 2004, with consequent reductions in their release into coastal waters (Ross et al. 2013).

Thus it appears there has been some reduction of PCBs in the marine food chain of SRKW habitat largely as a result of actions prior to 2003. Changes to ocean disposal guidelines in 2011 in Canada with respect to PCBs, are also expected to have a positive effect, although at the time of this review it is not clear if there is evidence of a further declining trend. Actions to restrict PBDEs that started as early as 2004 in the U.S. and came into force in Canada in 2008 and 2012 are expected to have a reduction effect but at the time of this review, it is not certain whether declining trends reported by Ross et al. (2013) are continuing.

Biological pollutants

Characterization of the threat

Biological pollutants, including pathogens and antibiotic-resistant bacteria resulting from human activities, may threaten the health of SRKWs, their habitat or their prey. Due to the small size of the southern resident killer whale population and the gregarious social nature of these animals, introduction of a highly virulent and transmissible pathogen has the potential to catastrophically affect the long-term viability of the population through reduced reproductive success and survival (Gaydos et al. 2004). Furthermore, although age may be a confounding factor, it has been suggested that there is an association between cetacean exposure to PCBs and mortality due to infectious diseases (O'Hara and O'Shea, 2001). Pathogens and antibiotic-resistant bacteria can enter the marine environment by means of coastal run-off and wastewater discharges.

A number of Recovery Measures have been proposed that involve reducing or mitigating the release of biological pollutants into the habitat, some are underway, others are not, (e.g., Recovery Measures 67, 81, 82, 59, 65) (Table 2). Canada's Wastewater System Effluent Regulations (WSER) of 2012 will require all wastewater facilities to meet the effluent quality standards by 2040. This would be expected to significantly reduce the release of biological pollutants, which is one of the recovery measures listed in the Action Plan. Highest risk facilities must be compliant by 2020.

Several measures that involve monitoring and identifying biological pollutant trends in SRKW are underway as part of ongoing long term programs. Presently most efforts are focussed on monitoring for pathogens and disease related mortality in stranded SRKWs and other marine mammals that inhabit the same region. The emergence of novel pathogens will be detected as part of these efforts. Standardized necropsy protocols and disease testing has been developed for BC and WA. This monitoring will also help to detect biological pollutants.

Effectiveness of actions

At the time of this review there is no indication that the threat of biological pollutants has been reduced, however it seems that biological pollutants are not as significant a concern as chemical pollutants. Nonetheless, compliance by Canadian wastewater treatment facilities may help reduce this threat when they come fully into force. Continued health monitoring via necropsies of dead SRKWs will continue to be important to detect emerging biological pollutants.

6.4 Ship Strike

Fast moving large vessels can pose a strike risk for whales, even killer whales. The recent mortality of J34, a prime age male found to have died from large blunt force trauma, highlights this threat. The very small size of the SRKW population and the low numbers of prime age males and females that support the reproductive potential and genetic diversity of the population means that a threat that could remove one animal will have significant consequences. There are no specific Recovery Measures to address this threat, because it was not identified as a threat during the recovery planning; related recommendations are contained in section 8 of this review.