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NOAA works help orcas by increasing prey availability, improving habitat quality, and conducting research on the orcas.

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Killer whales play a key role in the ecological and cultural fabric of the Pacific Northwest. Resident populations of killer whales in the Pacific Northwest saw steep declines in the early 1970s and have failed to recover even with increased management protection since then.

Initial support under the Killer Whale Research and Conservation Program is anticipated in the following three key strategies:

Increase prey availability - The Southern Resident population diet relies heavily on Pacific salmon, with Chinook salmon representing the majority of their summer diet, and other species including coho, chum, and steelhead being targeted in the spring and fall. The program will seek projects that increase the health of the salmon runs that are important for killer whales.

Improve habitat quality - The quality of killer whale habitat is affected by many different stressors including pollution and contaminants, and vessel traffic and noise. The program will support projects that reduce the source and the impact of these stressors, and therefore lead to improved habitat for killer whales.

Strengthen management through game-changing research - The program will support research projects that address information gaps and catalyze effective management actions in key areas, such as improving our monitoring of demographics and distribution, improving the health assessments of whales, and assessing the effectiveness of management interventions.

Through strategic partnerships and deployment of grant funding to the priority needs described above, the Killer Whale Research and Conservation Program seeks to increase our knowledge of killer whale populations and to help overcome barriers to recovery.

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Killer Whale Research and Conservation Program

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The Killer Whale Research and Conservation Program supports efforts to advance the knowledge and conservation of killer whales with a primary focus on activities that aid in the recovery of the Southern Resident killer whale Distinct Population Segment. The program may also support catalytic projects in other killer whale populations.

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There is an estimated 50,000 orcas globally.They are found in every ocean, making them the most widely distributed cetacean. They have also historically inhabited every ocean, but now the populations are more sparse.

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There is not sufficient data for many of the orca populations, but the Southern Resident population is considered endangered and the AT1 Transient population is considered depleted, as they were heavily affected by the Exxon Valdez spill. There are 7 left in this sub-population.

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They feed on sea birds, squid, octopuses, sharks, sting rays, fish, sea lions, and sea turtles. They are apex predators.

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They live in pods ranging from a few individuals to 20. Larger groups may temporarily form during mating season. They have coordinated hunting strategies. Resident orcas are matrilineal, with the oldest female leading the group.

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As apex predators, they exercise top-down control on the food chain. They are the biggest reason for mortality of sea lions. Without them, populations of their prey would soar. They also host endo and ectoparasites.

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People have hated and hunted these animals for a long time. Recently, attitudes have been shifting as people value their intelligence and their role in the ecosystem. Some people pay lots of money to see these animals in captivity while others believe that their role is in the ocean, where their impact will be felt.

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Attitudes, especially recently, have changed as well as the portrayal of the animal.

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Many in the Northwest consider the orca to be our region's unofficial mascot. But how did we come to love orcas so much in the first place? Environmental and International History Professor Jason Colby will be joining us on June 5 (just in time for Washington's Orca Awareness Month!) to take us on a deep dive into our society's intricate history with killer whales. In the meantime, Colby sat down with Town Hall's Alexander Eby to discuss all things orca-from etymology to questions about captivity to the rituals of our resident orca pods.
AE: I wanted to ask you about the title of your book, Orca: How We Came to Know and Love the Ocean's Greatest Predator. Can you tell me a little bit about that moniker, 'the ocean's greatest predator?'

JC: Well, the orca is really the undisputed apex predator of the ocean. When it comes to prey, they're specialist hunters. You've got so-called "transient" killer whales that focus on marine mammals: seals, sea lions, and even some smaller baleen whales. You have the salmon-eating specialists that are famous in our area and others that focus on sharks or stingrays. But everywhere in the world orcas eat what they want and nothing preys upon them.
AE: Are there any reported cases of orcas harming humans?
JC: There's one case of a young surfer who was bitten on the leg by a killer whale, but it was probably a case of mistaken identity-the whale probably thought he was a seal or sea lion. There was also a famous Arctic expedition in the early 20 th century where a photographer was on the ice and a pod of orcas approached him and started breaking the ice apart. It's possible they were just curious. It's possible they were investigating the expedition's dogs, thinking they were seals or sea lions. The photographer ran across the ice and got away safely, but that account was then published all over the world. It created this perception of the killer whale as an extraordinarily dangerous and formidable predator. There were certainly stories among sealers in Seattle and Victoria of dangerous encounters with killer whales, but no documented attacks that seemed intentional.
AE: If they don't typically harm humans, what earned them a name like "killer whale?"
JC: The origin of the name almost certainly comes from the Basque and then Spanish and Portuguese assassino de baleias, or "whale killer," which was likely transposed in English as "killer whale." That name would have originated among fishermen and whalers who saw orcas attacking much larger whales. If you step back to a period prior to when we saw these animals with affection and imagine what they looked like to the humans who had never seen them before-immense predators with jet-black skin and wolf-like teeth-it's understandable that we would find them frightening. Humans have a long history of being unsettled by sharp-toothed predators. It must have been pretty easy to imagine that we could wind up on the menu.

We use the name orca now, and we've convinced ourselves that it sounds friendlier and more complimentary than killer whale. But the name appears in the works of many 19th and early 20th century writers from a time when we still saw orcas as dangerous. These writers knew their Latin, and dubbing the whales "orca" was meant to convey a much more frightening image. In Latin, Orcinus Orca essentially means 'demon from the Netherworld.'
AE: That is rather evocative. But we don't think of them that way anymore. What's been responsible for the change in public opinion over the last few decades?
JC: Up until the early-to-mid 1960's this was a species that was still considered a potential threat to human beings. More importantly, this was a species that was viewed as a threat to more valuable resources like salmon and seals, which were being harvested for profit. Orcas were considered a vermin species, much in the same context of wolves, bears, and cougars across North America. It wasn't until the early to mid 1960's when the encounters with live killer whales in captivity began to transform public opinion. Seattle is really at the heart of this story. On Pier 56 there was a private Seattle Marine Aquarium, which no longer exists today. The aquarium's owner Ted Griffin was on a quest to befriend a killer whale.
AE: Was he one of the first ones to see orcas as intelligent creatures rather than just pests?
JC: There were others that were interested in observing them, but Griffin was the one who showed the world that they're intelligent creatures and potentially friendly to people. Canadian fisherman up north accidentally caught a couple of killer whales in their nets, and Griffin figured out a way to build a floating cage around one of these whales and bring it down to Seattle. This hundreds-of-miles-long journey of this floating cage became front-page headline news, not just in Seattle but across the world. Griffin traveled with this whale, which had been named "Namu," and they arrived in Seattle right before Seafair in 1965. And there was a massive celebration on the waterfront with a huge crowd gathered to welcome them.

Namu became the first whale to ever perform for people in public-and perhaps even more important is that Griffin himself became the first human being, that we know of, to swim with a killer whale. This was a revelation to people, to scientists and naturalists and writers. Most people thought that if he got in the water with this animal it would tear him apart. Instead he befriended this animal and started performing with it. This relationship, this connection between Griffin and Namu, was really transformative to the way the world saw this predator.
AE: Because killer whales became such an icon in this context of captivity, there's a complex discussion still going on about killer whales in captivity today. What's your perspective on killer whales in captivity?
JC: So the purpose of writing my book was to almost be a prequel to the 2013 documentary Blackfish, which was very successful in focusing people's attention on orca captivity. But the film was successful in part because people cared so much about orcas already. My aim was to tell the story of why we cared so much about orcas in the first place.

I always like to contextualize this historically. Keeping killer whales in captivity played a critical role in transforming people's views of this animal, but obviously the context of the 1960's and 70's is different from today. I think that most scientists now would say that the research that can be done on these animals in captivity has been done, so it's hard to make the argument that we need to keep killer whales in captivity to study them. But it's worth remembering that most of the killer whales in captivity in North America are captive-bred. I don't say that to diminish the animal rights question. Rather, I say it to point out that what happens with animals bred in captivity doesn't have a lot of bearing on the survival of killer whales in the wild.

I worry that the focus on the moral question of captivity takes attention away from the overarching threats to wild killer whale populations. Our region's resident killer whales used to number around 250 and now number at 76-and they're probably in an extinction spiral. The biggest threats to killer whales aren't aquariums or corporations in Orlando that are keeping a few orcas in captivity. With the growing prevalence of fisheries and pipelines, even here in the Northwest, there are factors that threaten killer whales on a much larger scale.

Food scarcity is a major issue due to growth of commercial fisheries and sport fishing. We also see pollution from increased tanker traffic contaminating their habitats-and even the noise from the tankers can be damaging. Orcas are acoustic animals, and the louder our waters get the more difficulty they have hunting and communicating. So as compelling as the moral question of captivity is to us, it's not related to these factors which I believe are a much greater threat to the species.
AE: Is there something that you wish people understood about orcas?
JC: One of the things that struck me as I studied orcas is that they are extraordinarily close-knit socially. Our resident Northwestern pods are multi-generational and matriarchal, with extraordinarily long-lived "grandmothers" who can lead their families for nearly a hundred years. Over that time these killer whale pods have developed their own traditions, memories, and itineraries of this region.

For example, take the northern resident killer whales who travel between mid Vancouver Island and southeast Alaska. When they return to northern Vancouver Island in summer they visit these beaches-"rubbing beaches," people call them-where they take turns rubbing up against these small round rocks. Their visits to this "whale spa" have been observed for generations.

And of course the southern residents have their own rituals. Probably their most famous one is the "greeting ceremony." The southern residents have three distinct pods: J, K, and L. When the pods come together they line up abreast a few hundred yards apart and pause for a few minutes, then suddenly bolt forward into this large frolic. It's really fascinating to watch.

They're remarkably sophisticated animals with their own cultures, their own rituals, their own memories. And I do wonder how they interpret the changes that we've imposed on their ecosystem. It's been transformed incredibly rapidly in a short period of time, and one wonders what they make of it.
Don't miss Jason's event on Tuesday, June 5. Get your tickets here.

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Fearsome to Friendly:Our History with the Orca

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Many in the Northwest consider the orca to be our region's unofficial mascot. But how did we come to love orcas so much in the first place? Environmental and International History Professor Jason Colby will be joining us on June 5 (just in time for Washington's Orca Awareness Month!)

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More sympathy is growing for captive orcas

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The effect of "Blackfish", research article

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The effect of "Blackfish", research article

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This documentary contributed to Sea World's elimination of their breeding program in 3 years.

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Communication, Northern Arizona University, Flagstaff, AZ, USA

The documentary film Blackfish (2013; www.blackfishmovie.com) follows Tilikum, a captive SeaWorld prisoner-orca responsible for the death of trainer Dawn Brancheau and two others. The film has had a profound effect on public perceptions of orca captivity creating the "Blackfish Effect." Our critical analysis of the film engages Plec's (2013) internatural communication categories of complicity, implication, and coherence. We argue that the film illustrates the flawed hierarchy within the binary/dualistic system. In deconstructing a dualism, we must recognize the physical power and actions of captive orcas that could be seen as a form of protest rhetoric. The case example of orcas in captivity as a whole illustrates that regarding orcas as unique actors with intelligible behaviors offers a way of understanding how to listen to the more-than-human world. Our article has been one attempt to illustrate how captive orcas can be heard as extra-human citizens who participate, and even instigate, policy making.

Arguably one of the most impactful and successful documentary films, Blackfish fundamentally contributed to the elimination of SeaWorld's breeding program in less than 3 years. In a National Public Radio interview on March 17, 2016, SeaWorld President and CEO Joel Mamby collaborated with the Humane Society of the United States after just 10 months of working for the company to announce that SeaWorld had agreed to stop breeding orcas in captivity and would be phasing out all orca performances by 2019 ( SeaWorld to End Orca Breeding Program in Partnership with the Humane Society, 2016). The protagonist of Blackfish is Tilikum, a 12,000-pound bull orca who has been held captive for the past 29 years in SeaWorld Orlando. Responsible for the deaths of three people, his most recent victim was Dawn Brancheau, an experienced SeaWorld trainer, who was killed in February of 2010. In the film, her death is presented as a human tragedy that could have been prevented by not subjecting the whale to the cruelty of confinement in the first place ( Chang, 2013, para. 2). CNN broadcast Blackfish in 2013 and 6 months after airing it had been watched by roughly 25 million viewers ( Kaufman, 2014). Sparking a subset of the environmental justice movement informally dubbed the "Blackfish Effect," the film surprised many with its significant impact on SeaWorld's revenues, stock value, and most recently, its breeding program. Perhaps even more importantly, the film has had a profound effect on public perceptions of captivity, orca health as an apex predator, and related environmental issues. Unlike other "more-than-human" ( Abram, 1996) animal documentaries, the "Blackfish Effect" has been sustained through social media sites like Facebook and Twitter and has continued to draw support. The "Blackfish Effect" emerged through a multi-platform social media reaction as a colloquial term to categorize the many forms of responses to the film. These responses included but were not limited to memes, policy changes, and protests.

In what follows, we discuss the film and the "Blackfish Effect" thematically through an "internatural communication" ( Plec, 2013) lens. We view the "Blackfish Effect" and the film Blackfish simultaneously, recognizing that the two are linked in a mediated process as the "Blackfish Effect" is an extension of the film itself. In Perspectives on Human-Animal Communication, editor Emily Plec (2013) defines internatural communication as "the exchange of intentional energy between humans and other animals as well as communication among animals and other forms of life" (p. 6). Internatural communication is intended to be inclusive of previous terms used in environmental communication (e.g., biorhetoric, transhuman communication, and corporeal rhetoric) but seeks to expand and embrace new understandings of human and more-than-human dialogs. In addition, we deliberately shift between terms like extra-human ( Peterson et al., 2007), other-than-human, and more-than-human ( Abram, 1996). While "extra-human" may imply human plus, "more-than-human" incorporates a hierarchy that reverses the current paradigm of humans over animals. "Other-than-human" (perhaps closest to "non-human") indicates entities as different-than-human and can be read as lacking/negative, and we use it strategically only when referencing beings forced into subordination or discussing humans exercising power over animals.

Plec's (2013) anthology is organized around three ideas/categories: complicity, implication, and coherence. Complicity looks at how humans exercise power over other-than-human entities. Implication asks humans to reflect and re-engage in a new relationship with the more-than-human world. Coherence explores the shift to a new paradigm where interconnection and cyclical/systems thinking becomes the norm. These categories are an organizing structure for her book; however, we use these ideas methodologically to build a coherence framework via our case study and analysis of Blackfish and the "Blackfish Effect." Because this documentary has had such a profound effect, it is imperative for environmental activists and policymakers alike to understand what makes this film stand out from other environmental documentaries and how it may offer a prescriptive framework for environmental activists. We argue that the film illustrates the flawed hierarchy within the binary/dualistic system. This happens by dismantling the ideas of "power-over" (i.e., humans having power over other-than-humans) because the case of Tilikum and his respective murders proves the impossibility of the "power-over" ideology. Breaking down a dualism is not just a matter of symbolic interpretation but of material recognition, as Blackfish reveals. Put differently, deconstructing a dualism is not simply about a moral construction but must be a recognition of the physical power and actions of captive orcas and could be seen as a form of protest rhetoric. We argue that the case study of orcas in captivity as a whole illustrates systems thinking versus dualistic models, which in turn shows coherence as a way to "hear" internatural communication.

Our methodological approach to viewing the film uses a thematic analysis to draw out salient narratives. While we engage in textual analysis, we also understand that we are audience members/consumers affected by the film. In short, it is important to remember that critics have assumptions that they cannot easily separate from their frame of reference when exploring texts. As such, we attempted to be self-reflective throughout the writing of this essay by continually returning to Plec's frames for our analysis. Through Plec's above categories, we explore how these frames are expressed in the documentary. First, complicity is shown in the film by illustrating that SeaWorld depicts orcas in captivity as either happy or necessary for scientific research. Furthermore, publics who attend SeaWorld theme parks are also part of the complicity narrative. Second, through the lens of implication, Blackfish critiques SeaWorld's dominant position by proposing an alternative narrative of psychosis, which argues that Tilikum's outbursts and neurosis (e.g., killing, grinding/breaking teeth on the cage bars) are symptoms of posttraumatic stress disorder perpetrated by his prison-like living conditions. Finally, the third lens brings to light a new paradigm of internatural communication where Tilikum and other captive orcas are seen as their own agents and as such, their voices and actions would be heard as a clear choice to be freed (sea pens, release to the wild, etc.). We argue that the shift to coherence is what contributes to the "Blackfish Effect" or a sustained movement demanding the release of Tilikum and others like him. Using this lens, his homicidal acts are not a symptom of psychosis that can be fixed with, for example, a larger and more visually pleasing pen (as proposed by SeaWorld). Rather, Tilikum's actions disrupt complicity and implication and can be read as a "symbolic declaration of war" ( Milstein, 2013, p. 177), creating a breach that bridges the divide of human/orca communication by illustrating alternative symbolics ( Schutten and Rogers, 2011). Our paper expands internatural communication dialogs by illustrating how to recognize new symbol systems via the public screen ( DeLuca and Peeples, 2002) by placing equal value on more-than-human "voices" in anti-captivity rhetoric even when the "symbols" are not linguistic.

Blackfish, the "Blackfish Effect," and Documentary Film as Connective Action

Blackfish, directed by Gabriela Cowperthwaite, was shown at the Sundance Film Festival in 2012 and acquired by Magnolia Pictures and CNN Films. Due to their global charismatic megafauna status, Milstein (2009) refers to orcas as "boundary creatures," which symbolize a "potentially enlightened and harmonious humanature" (p. 97) where "tourists" or audience members often leave an encounter with a sense of connection and, potentially, leave as an advocate for new "ecocultural alliances" (p. 97). Seen in this light, Blackfish from its inception presented engaging subject matter that would appeal to a large audience. It is also widely understood that popular nature documentaries typically focus on environmental use-value that specifically "encode and (re)code anything back into the logic of capitalism" ( McHendry, 2012, p. 145). Framing nature in terms of its use-value maintains the subject (human)/object (nature) binary. As such, it becomes even more important to examine media texts that challenge ideologies that do not constitute nature as a resource for human use ( Schutten, 2006, 2008).

Nature documentaries as a genre have the potential to encourage pro-environmental behavior. Documentaries allow for more accessible exposure to many types of nature encounters in a way that is less expensive, less time consuming, and more readily available as compared to zoos or other direct nature experiences ( Arendt and Matthes, 2016). Similarly, Pezzullo (2007) writes "the use of documentaries by social movements to "mobilize viewers" with "a committed eye" positions them as desirable and potentially efficacious modes of communication that are relatively more affordable to circulate with broader audiences" (pp. 144-145). Blackfish presents a perspective of reality that can be "perceived to be an expansion of human vision, a means of entering into a world that was invisible to the human eye..." ( Horak, 2006, p. 459). The film splices together scenes of Tilikum's perceived reality and other orcas, unveiling a much different picture than what entertainment parks portray publicly.

Scholars have argued that nature documentaries contribute to environmental knowledge gain and attitude change ( Holbert et al., 2003; Barbas et al., 2009). In the instance of Blackfish, nature documentaries emphasizing cetaceans may contribute to increased knowledge about whales and whale habitat despite the central foci being on captive whales. However, does this heightened knowledge translate into pro-environmental action? Arendt and Matthes (2016) examine how a mediated nature experience such as a documentary could have a positive influence on an audience's environmental behaviors, including increased giving behavior. We extend their work, claiming that financial donation might not be the only measure of public participation but adding that social media participation or "e-tactics" ( Katz-Kimchi and Manosevitch, 2015) could also be viewed as a form of direct action and pro-environmental behavior. In this way, documentary film and other forms of media that potentially offer audiences alternative structures of meaning for understanding their internatural relationship become part of an ongoing sustained environmental justice movement such as the "Blackfish Effect." As the Oceanic Preservation Society (OPS) wrote in a meme, "A film can be the most powerful weapon in the world-a weapon of mass construction."

In looking at how texts influenced the "Blackfish Effect" and participated in the environmental justice movement, it is first helpful to define environmental justice. Bullard writes "the goal of an environmental justice framework is to make environmental protection more democratic. More importantly, it brings to the surface the ethical and political questions of 'who gets what, why, and in what amount'" [as cited in Pezzullo (2001), p. 2]. Environmental justice frameworks illustrate the need for public participation in order to further democratic processes and highlight marginalized groups and their lack of access to such processes. To this end, Pezzullo (2001) writes that environmental communication must continue to focus on citizen participation in environmental/political decision-making. While environmental justice cases have historically focused on human-centric issues, our study extends the umbrella of citizen to include more-than-human "voices."

In Blackfish, there are multiple discourses surrounding the murder of Dawn Brancheau. SeaWorld has gone on record placing blame on Brancheau for making various mistakes during the performance (e.g., having a her hair in a ponytail) and in turn, continues to defend the imprisonment of Tilikum and other orcas. Alternative narratives from trainers and other experts in the film posit that the events were not Brancheau's fault but rather caused by Tilikum's psychosis due to his captivity. While oppositional, both narratives from the film are similar in that they ignore Tilikum's agency and mitigate his ability to act with intention. Despite these narratives, the audience is repeatedly asked to witness the esthetically disturbing stories of three visceral murders by Tilikum and several attacks by captive orcas.

There are moments in the film that breach normative discursive narratives of human-orca communication. For example, the film dispels the potential misconception that orcas, culturally labeled "killer whales," are not actually killers of humans in the wild. In fact, the only incidents of attack and killing on record have been by orcas in captivity. An audience's consciousness can shift to acknowledge that orcas are not "killers" of humans in the wild, but become "killers" due to imprisonment. These breaches of perception can be seen as moments of audience identification with captive orcas where witnessing is in motion. In discussing witnessing as a rhetorical practice, Pezzullo (2007) writes, "Rather than maintaining a distance gaze through which we ignore atrocities, witnessing suggests the need to explore 'what we are trained to overlook.' In this act of seeing, the witness risks identification with the fate of other people, places, and events" (p. 147). Expanding on Pezzullo's study exploring people, places, and events related to witnessing, Schutten (2011) writes "a truly inclusive biospheric literacy must include the pain of other-than-humans as well as humans. Our imagined communities must go beyond human-centered epistemologies and injustices and be able to comprehend the cries of the concrete, material earth that surrounds us" (p. 347). To this end, witnessing does not end at the visual but includes embodied experiences for both human and more-than-human entities. The witness not only sees but also feels embodied pain that allows for identification with the subject. Blackfish utilizes this rhetorical strategy telling the story of Tilikum and evoking embodied experiences that often activate empathy and contribute to an alternative perspective highlighting the consequences of captivity.

This act of witnessing may cause what Milstein and Kroløkke (2012) refer to as a rupture. Ruptures could illustrate how "communicative moments (in the film) might point us to new understandings about the intersections of nature, culture, and the body" (p. 83). In reference to these ruptures, we have chosen to model our language after a whale/orca term, "breach," in an effort to have our language mirror more-than-human behavior. These breaches might create "boundary transgressing moments" ( Milstein and Kroløkke, 2012) of witness for the audience moving them from complicity into implication and eventually toward coherence, as we will discuss later. It is the move into coherence that we argue has sustained the movement and created the "Blackfish Effect."

Since the broadcast of Blackfish, continued public pressure has instigated several blows to SeaWorld. On the legislative end, new policies have been proposed such as the Orca Welfare and Safety Act in San Diego, California, which would make it illegal to "hold in captivity, or use, a wild-caught or captive-bred orca for performance or entertainment purposes" ( Kirby, 2014). In addition to policy change, the film has also initiated grassroots responses to, and boycotts of, the SeaWorld Corporation. The company has felt the effects of consumer losses in lost revenues each consecutive quarter since the film's release. According to a public press release from SeaWorld Entertainment, Inc., there were one million fewer visitors to the park in 2014 than 2013, and yearly revenue dropped by over 80 million dollars ( SeaWorld Entertainment, Inc., 2015). Since Blackfish was released in 2013, SeaWorld's stock prices have plummeted over 50 percent and continue to fall ( Udland, 2014, para. 7). Further threatening the corporation's public financial health is a class action lawsuit lead by investor Lou Baker claiming the company failed to inform investors about the potential impact of the documentary and the park practices brought to light in the film ( Enlow, 2014, para. 7).

These consumer losses can be linked to the prevalence of social media and public participation. This aspect of the "Blackfish Effect" has significantly contributed to the public relations crisis SeaWorld has faced since the release and widespread viewing of the film on CNN. The film sparked an online social media presence including collaborative efforts between Blackfish's Facebook fan page, The OPS, People for the Ethical Treatment of Animals (PETA), the film Racing to Extinction's Facebook page, Cetacean Inspiration, Ric O'Barry's Dolphin Project, and more that are continually growing and evolving. Discussing the effect of Internet memes as delegitimizing discourse to corporate credibility, Davis et al. (2015) writes, "Social media, memes, online cultural play, and the ease of sharing have all made quick responses to corporate actions and policy easier with a higher potential for potency and resonance" (p. 19). The Internet becomes a "great equalizer" that allows environmental justice organizations with limited resources to delegitimize corporate responses ( Davis et al., 2015). In this way, following Katz-Kimchi and Manosevitch (2015), we can see new social movement actors, often critiqued for passive observation, engaging as active participants in a multitude of environmental conversations via "e-tactics." E-tactics are defined as mobilizing structures that "provide users quick, easy, and familiar means to actively support the campaign" ( Katz-Kimchi and Manosevitch, 2015, pp. 258-259). For example, the ability to "like," "share," and "re-tweet" are forms of active participation.

Complicity and Implication in Blackfish

As a corporation, SeaWorld has a vested interest in maintaining its audience's participation in complicity. The captivity model props up human interest/entertainment and financial investments as a legitimizing rationale for the subordination of other-than-human animals. To this end, in the film (and trailer), we hear a former trainer say "the industry has a vested interest in spinning these (incidents/attacks). It sells a lot of Shamu dolls, sells a lot of tickets at the gate" ( Blackfish). The first justification SeaWorld makes is that they are leading innovators in oceanic animal conservation, reinforcing, and justifying the binary/dualism of humans over other-than-humans for purposes of human education. The second justification SeaWorld perpetuates, according to the film, is that any error is not due to the effects of captivity or the animals being "out of control" but rather individual trainer error. SeaWorld rhetorically removes the orca's involvement from the situation, protecting their investment, claiming that the trainer "drowned," or in the case of Brancheau, they first said that she "slipped and fell" and later claimed that it was her ponytail that caused Tilikum to murder her. The next defensive tactic the film critiques is that SeaWorld highlights the trainer's mistakes: "He was supposed to get off the whale" ( Blackfish). SeaWorld defends its legitimacy as a company by stating that in the case of the murder of Alex Martinez at Spain's Loro Parque ("Parrot Park"), there was an "accident" and "nothing we could do," despite autopsy evidence showing this incident as a "brutal attack" ( Blackfish), as shown by the compression fractures, bite marks, and tears to vital organs.

In addition to showing how SeaWorld claims to be a force in environmental education and that large mammal incidents were "accidents," the film also shows that SeaWorld had multiple "scripts" or narratives that they instructed their trainers and employees to recite. In this sense, the film illustrates that trainers feel some responsibility for remaining complicit. For example, one trainer interviewed in the film confessed that she was embarrassed by what she had to say to tourists in the park and as a part of the orca show. She remembered parts of her script like: "Namu is doing that because she wants to, not because she has to." Other examples from the film include discussion of orca whale mortality rates in captivity. The film shows clips of three SeaWorld employees saying that orca lifespans in captivity are 25-35 years and longer than those in the wild, and one trainer is filmed saying, "They're documented in the wild living to be about 35, mid-thirties. They tend to live a lot longer in this environment because they have all of the veterinary care" ( Blackfish). Orca researcher and producer of Blackfish, Howard Garrett claims this is not true. In an interview during the film, he responds by saying, "And of course that's false. We knew by 1980 after half a dozen years of research that they live equivalent to human life spans, and every other potentially embarrassing fact is twisted and turned and denied one way or another." He explains SeaWorld's script, stating: "because the whales in their pools die young, they like to say that all orcas die at 25-30 years" ( Blackfish).

In these examples, attempts are made by SeaWorld and its employees to dismiss the artificial boundaries put in place by captivity. This framing follows what Milstein (2013) found in her study of "zoo'd" gorillas where they were positioned as agents that choose, enjoy, or benefit from captivity rather than "unconsenting captives and victims of unsustainable global human practices" (p. 178). She goes on: "A slave-master narrative is evidenced throughout the guide's discursive reframing: why would they want to leave? We're nice to them, give them a nice space, feed them, etc." (p. 178). The tour guides Milstein studied at the zoo are akin to the trainers and other employees at SeaWorld.

The film clips of the tour guides/SeaWorld staff justifying captivity are juxtaposed to follow-up interviews with trainers who appear to feel remorseful, embarrassed, sad, and guilty about their part in keeping up SeaWorld's "front of the house" performance. The film makes clear that the trainers now know how much they bought into what SeaWorld told them. It is at this point that the film shifts from illustrating examples of complicity to implication. Implication is defined by Plec (2013) as "a critical awareness and effort to understand and make our role as humans in communicative relationships and interactions with other animals more just and responsible" (p. 7). To this end, audiences are told that trainers felt remorse but chose to stay working at SeaWorld because they felt they had to. One trainer commented they felt sorry for Tilikum because, "if they leave, who will take care of him."

These scenes in the film work to create a witnessing opportunity that presents captivity as wrong. The first move to making this argument is the "orca-knapping" scene. The audience meets John Crowe who hunted and captured Tilikum in Puget Sound, Washington, 1970. We quote this scene to show Crowe's complicity in commodity capitalism in marine entertainment, along with his awareness and regret illustrating his implication in the event.

We're there trying to get the orca in the stretcher and the whole fam damily [ sic] is there 25 yards away may be in a big line and they're communicating back and forth. Well, you understand then what you're doing (Pause). I ... I lost it. I just started crying. I didn't stop working, but I ... you know ... I just couldn't handle it. Just like kidnapping a little kid away from its mother. Everybody's watching, what can you do? It's the worst thing I can think of. I can't think of anything worse than that. This really sounds bad but when the whole hunt was over there were three dead whales in the net. So they had Peter, Brian, and I cut the whales open, fill them up with rocks and put anchors on their tails and sink them. Well (pause), really I didn't even think about it being illegal at that point. I thought it was a PR thing ... I've been part of a revolution and the change of presidents in Central and South America and seen some things that it's hard to believe. But this is the worst thing that I've ever done, is hunt that whale ( Blackfish).

Crowe remembers crying during this orca-knapping. His "confession" of this to the viewer exposes an embodied witnessing rhetoric that may create a breach for the audience. Crowe believed the whales were communicating to each other. He expresses a view indicating that the whales had conscious awareness while witnessing the taking of their children. This is exemplified by the fact that when the young ones were corralled they stayed, even though they could have left and protected themselves from any potential harm from the hunters. To this end, Howard Garrett prefaces this scene with Crowe by stating that the captors were throwing bombs in the water to herd the whales, "but the orcas had been caught before and they knew what was going on and they knew their young ones would be taken from them" ( Blackfish). Both of these men confidently discuss orca intelligence as identifiable with human intelligence. As such, in line with various campaigns and responses, the audience may view captured orcas as prisoners. Viewing orcas as prisoners allows the audience to move into implication, seeing trainers and employees as prison guards. Moreover, all those involved with every stage of captivity, from capture to passive marine park tourist, are culpable. Seen in this light, passive tourism becomes an active part in the oppressive system of imprisonment and may also be a moment where audience members shift from complicity to implication. Supporting this claim, former senior orca trainer John Hargrove (2015) writes in his book Beneath the Surface: Killer Whales, SeaWorld, and the Truth beyond Blackfish:

Imagine the situation [captivity] in human terms and the closest institutions that come to mind is a prison, where the inmates are completely dependent on the guards and the system to provide them with the basic needs of life: food and water. It is a terrifying and depressing metaphor for trainers who love the whales and who feel responsible for them. Why? Even in the analogy, even if the prisoner-whale decides that it likes some of the guards better than others, in the end, they are all still guards, part of the same system that oppresses them. You can be a prisoner and genuinely like a specific prison guard-and that prison guard may genuinely like you-but that doesn't take away the fact that you're in prison ( Hargrove, 2015, p. 77).

There are currently 56 known "prisoner-whales" in captivity worldwide ( Whale and Dolphin Conservation, n.d.). The film does not just blame SeaWorld or their trainers as responsible for maintaining the prison, but implicates the public (e.g., tourists, spectators, and park visitors) as a part of the prison system as a whole. An important element of the prisoner metaphor is that it opens up understandings of other-than-human captivity as problematic entertainment. Orcas held against their will, in prison-like conditions, cannot be viewed as "happy" or "healthy." Rather, the film presents another narrative about captivity, claiming that it leads to psychosis. Psychosis is a result of the orca's living conditions in small cells, and effectually, psychosis is the cause for Tilikum's (and other orcas) attacks. One example was described in the film from the portion of Tilikum's life when he was imprisoned at Sealand in Canada. Audiences hear from the Sealand owner and former trainer that the trainers would withhold food to coerce the whales into the evening modules and, if they went in, they would get to eat. Tilikum would spend from 5:00 p.m. until 7:00 a.m. in a small, dark, module cell and the two female whales he was imprisoned with would "rake" (scraping their teeth on his flesh) him in the night. Blackfish takes on the perspective of the whale-prisoner and allows the audience to "feel" their captivity. Another clip, taken from a CNN news spot, shows anchor Jane Velez-Mitchell responding to one of Tilikum's attacks: "If you were in a bathtub for 25 years, don't you think you'd get a little psychotic?" ( Blackfish). These scenes focus on Tilikum's experience at Sealand, emphasizing his confinement, isolation, and abuse by his fellow prisoners. This arguably led to his psychosis, resulting in the murder of Kelty Burn on February 21, 1991, in Victoria, British Columbia, the first of Tilikum's three homicides. Ex-trainer Samantha Berg comments in the film, "Tilikum is not an evil animal-he is a highly intelligent, emotionally complex mammal. And we've made him psychotic" (Blackfish). Tilikum's actions could be dismissed as a case of "one bad apple," however, the film makes clear that there have been several prisoner-whales that have violently attacked and injured human trainers. Other parts of the film discuss the indicators of psychosis or mental distress by showing how the whale-prisoners often gnaw on their enclosures, bang on their pens, and attack each other, leading to health issues like severe tooth and stomach problems.

The psychosis narrative is a result of understanding captivity as imprisonment and is important because it shifts the discussion of captivity from being necessary, healthy, or important for environmental advocacy as SeaWorld claims. It instead highlights captivity as "unnatural" and damaging to the orcas, and moreover, dangerous for trainers (prison guards) working with the orcas. The psychosis narrative may also be important in the implication stage of understanding human-orca communication, as it implicates human spectators and tourists as being partially responsible for orca imprisonment. At the same time, however, the psychosis narrative still mitigates or overlooks the orcas' agency in their own actions. It suggests that the attacks are the direct effects of mental illness, as though the orcas could not control how they acted. As such, captivity is presented as only being a problem because of the health issues it creates. This narrative may be important, but we contend that it is not what allows for a sustained "Blackfish Effect." The psychosis narrative does not necessitate the "freeing" of these orcas, but rather allows for potential other solutions, i.e., a bigger pool enclosure and more area to swim. However, the response to the film shows that audiences are not satisfied with SeaWorld's proposals for bigger pools. Rather, they demand exoneration.

Tilikum's attacks were not simply a result of psychosis. Orcas should be acknowledged as intelligent and active agents. We read them as intentional revolutionaries struggling against their prison guards. Following an internatural communication paradigm, these actions should be embraced and witnessed as an intentional demand for release. Here, the film teaches audience how the binary is inverted, both materially (Tilikum's physical control over his victims) and symbolically (interpreting Tilikum's actions as deliberate calls for release). It is this agency that we want to highlight as being important for the move from implication to coherence and new internatural understandings of human-orca communication.

Violent Spectacle: Shifting to Coherence

Milstein (2011) finds that most western discourse on humannature relationships is framed in a way that presents humans as agents and nature, in this case whales, as objects. However, Tilikum's story in Blackfish positions him as an active agent who potentially chooses when and how to perform "violent" spectacle. It is important to note here that the six major attacks by prisoner-orcas discussed in the film are all performed in front of public audiences except for one. In trying to hear different voices of the other ( Carbaugh, 1999), we contend that these public performances of power are intentional and illustrative of a "speaking" voice utilizing alternative symbolics. Plec (2013) writes about "the possibilities of a coherence theory of human-animal relations ... for repositioning our human ways of communicating and knowing alongside rather than above those of other animals" (p. 7). The human voices in Blackfish (except for one expert witness in Brancheau's court proceedings) indicate that the power-over model of captivity is no longer justified for a variety of reasons. The documentary's emphasis of grotesque and horrifying whale attacks and murder scenes brings to the surface discourses of human exceptionalism. The captivity and, in turn, torturous reality of orcas becomes extremely problematic for viewers as the film claims that orcas are sentient beings like humans. The comparison of humans as nearly identical to orcas, combined with the chaos of trainer incidents, helps to shift the audience toward a coherence paradigm that sees the "freak show" and "horror" aspects of captivity.

A statement appearing on the Blackfish official film site states: "A mesmerizing psychological thriller with a killer whale at its center, Blackfish is the first film since Grizzly Man to show how nature can get revenge on man when pushed to its limits" ( http://blackfishmovie.com). Hailing Grizzly Man in this comment draws explicit connections between the two films, illustrating the perceived consequences of human interactions with charismatic megafauna that have been pushed to their limits and are seeking revenge against "man." Schutten (2008) in her analysis of the documentary Grizzly Man writes about the predator/prey relationship and the nature/culture binary that posits humans as objects rather than subjects and "forcibly moves humans to the nature side of the dualism, thereby questioning the superiority of the culture side of the binary by exposing human vulnerability" (p. 195). We argue that the discomfort felt by some viewers to Treadwell's death is similar to the dissonance felt by audiences to Brancheau's death. Both of these films captivate audiences and are posited as psychological thrillers highlighting human vulnerabilities. Blackfish could be read as an example of audiences interpreting or understanding, in some way, internatural communication.

One such scene in the film shows an attack on Ken Peters, an experienced trainer working at SeaWorld in 2006. Peters was preparing for a "rocket hop" with Kasatka, a 5,000 lb orca. This segment begins with a clip from The Today Show where anchors introduce the story by saying, "A SeaWorld trainer is recovering today after a terrifying ordeal in front of a horrified audience" ( Blackfish). Next, the viewer sees the happy and enthusiastic trainers working with the orcas while SeaWorld's signature upbeat show tunes play in the background. We then read text saying, "Seconds after diving in, Kasatka seizes Ken's foot" ( Blackfish). This scene takes a dramatic shift at this moment as an ominous, eerie, musical soundtrack begins playing. The music is reminiscent of the attack scenes from the oceanic thriller Jaws (1975). We quote the narration at length here to illustrate the conscious will of orcas like Kasatka:

[Kasatka] dragged him to the bottom of the pool. And held him at the bottom. Let him go. Picked him up. Took him down again. And these periods he was taken down were pretty close to the mark. You know, minute. Minute twenty. When he was at the surface, he didn't panic, he didn't thrash, he didn't scream. Maybe he's just built that way but he, uh, he stroked the whale. And the whale let go of one foot and grabbed the other. That's a pretty deep pool and he took him right down....He [Peters] knew what he was doing because when, you can see him actually in the film, the def is so good you can see him ventilating really hard so he knows about swimming and diving and being underwater, he may have been assuming he was going under again. I did not walk away unimpressed by his calm demeanor during that whole affair. I would be scared shitless. He was near to the end. Presumably, Ken Peters had a relationship with this whale. Maybe he did and maybe that's what saved him but Peters got the whale to let him go. And they strung a net across. And Ken Peters pulled himself over the floatline and swam like a demon to the slide out because the whale was coming right behind him. The whale jumped over it and came right after him. He tried to stand up and run but of course his feet were damaged, I mean he just fell. Scrambled ( Cowperthwaite and Oteyza, 2013).

It is interesting to note the commentary by Duffus in the beginning of this scene because he seems to be indicating that Kasatka knew how long she was taking him down as she was conscious of the "mark" in which Peters would drown. To this end, Hargrove (2015) discusses orca's use of echolocation in the wild. He writes, "their sonar allows them to sense the heart rate and breathing of their prey. It helps the whales strategize their final kill" (p. 89). In captivity, this ability helps whales locate and find their trainer for their performances. In other words, this comment is illustrative of Kasatka's intelligence and ability to use her senses to make a choice about whether or not to kill Peters.

The overarching visual representation of this scene disrupts the normative SeaWorld performance because Kasatka is intentionally exerting authority over the situation, disrupting the binary, and manipulating or even "playing with" her trainer, taking back physical control of the performance. Additionally, this scene counters the position that captive orcas do not intentionally attack their captors. They can and will. As a marine-loving culture, we often refuse to believe that Kasatka had agency in this example and rather see the scene as SeaWorld depicts it viewing orcas as either innocent in the event (blaming the trainer's mistakes), or as Blackfish depicts the orcas as "sick" and damaged from psychosis and as such only "attacking" because they are "crazy" and not out of intentional will. Our point then is to illustrate how we can understand and interpret these events as internatural communication. In acknowledging an alternative symbolic, we should listen and respond to the orca's clear communication, rather than try to explain it away as "hysterical" psychosis or an exceptional, out-of-the-ordinary event. We argue that the audience has the potential to interpret the film, like this scene discussed, as internatural communication, i.e., Kasatka's legitimate communication.

In addition to the agency read into Kasatka's attack, Blackfish further illustrates the intention behind Tilikum's second murder of Daniel Dukes on July seventh, 1999, which could have arguably been done for "show." Splicing together the narrative with two ex-trainers, Jeffrey Ventre and John Jett, viewers are presented with Dukes' account as they both describe SeaWorld's public relations perspective on the tragedy:

[It was a] perfect storyline, a mentally disturbed guy hides in the park after hours, and strips his clothes off and decides he wants to have a magical experience with the orca and drowns because he became hypothermic. So, that's the storyline and none of us were there to know the difference... One of the employees, I don't know if it was a physical therapist or somebody with, coming in the morning and there was Tilikum with a dead naked guy on his back, kind of parading him around the back pool. The public relations spin on this was that he was kind of a drifter who died of hypothermia but the medical examiner reports were more graphic than that. For example, Tilikum stripped him, bit off his genitals, there was bite marks all over his body ( Blackfish).

The use of the descriptor "parading" here is of interest. Parading points to the metaphor of circus performance built into SeaWorld's image. Milstein (2016) analyzes how the "performer metaphor" constitutes "star making fetishism" (p. 230) where tourists view the wild Southern Resident Killer Whales (SRKW) and often view what they are watching as a "show" that "situated wild nature as intentionally exhibiting for humans" (p. 233). The performer metaphor, while representing an "intense human-whale association, it simultaneously constituted anthropocentric detachment" ( Milstein, 2016, p. 232). In profit-based marine amusement parks, the performer metaphor is a key part of the experience, conditioning viewers to see the "circus" in which orcas are the stars of the show. Here, the term parading illustrates how deeply ingrained the performance metaphor is for witnesses. Orca flips and spy-hops are viewed in the same way as the murder-as a performance.

The SeaWorld performer metaphor extends into the "wild" as Milstein (2016) looks at how audiences of whale-watching tours often view the whales in the same light as places such as SeaWorld. These tourists often claim that the wild orcas chose to come near the boat to put on a "show" for the particular tourists, that they were "chosen." With prisoner-whales, the performer metaphor seems to be so routine that both Ventre and Jett used it to describe this attack via Tilikum's parading. Interpreting this as more than a coincidental word choice, this scene exhibits how Tilikum executed his attack. He did not simply murder Dukes. Rather, as he was trained and coerced to perform daily in front of an audience, Tilikum performs with Duke's body, "parading" him around until morning. This potential choice by Tilikum disrupts the popular notion of killer whales as "pool toys" ( Morton, 2002), reasserting their position as apex predator. One could interpret this as a feeling of pride, a "voice" of sorts from Tilikum via his predatory performance that illustrates his agency.

The final example of disruption of the binary/dualism that we discuss is that of Dawn Brancheau's death on February 24, 2010 at SeaWorld Orlando. The film opens with a voice recording of the 911 call:

Operator: Orange County Sheriff's Office

Caller: We need a-response for a dead person at SeaWorld. A whale has eaten one of the trainers.

Operator: A whale ate one of the trainers?

Caller: That's correct ( Blackfish).

The audience hears dissonance and hesitation in the voices of both people on the phone that seems to center on the disruption brought about by the word choice of "eaten." To this end, Schutten (2008) writes, "seeing a human animal become food for "wild" animals interrupts the narrative that humans are above animals" (p. 205). Tilikum did not necessarily "eat" Brancheau, yet, this is the word choice of the 911 caller, indicating dissonance felt by the predator/prey relationship being disrupted. This illustrates that the humans watching recognized the disruption in an artificial atmosphere where we forget we are prey, inverting the hierarchy where humans are seen as superior and in control. Furthermore, the imagined sight of teeth on skin in the act of eating a human may create a visceral effect constructing an embodied experience of what it may mean to feel like prey. News of Brancheau's death spread quickly to the other SeaWorld parks. According to Hargrove:

They were gathering all the trainers at the Texas park. [And they told us] "There's been an accident at the Florida park and a trainer was killed" [then we were told] "and he [Tilikum] still has her." And I just was so disturbed by that and the reality of how powerless we are ( Blackfish).

Hargrove's realization of his powerlessness brings to light how Milstein (2009) discusses zoos and animals in captivity in terms of power and the human gaze. She explains that the "exhibition of animals" as the "central function of zoos, is a process of power" determined by the visitor's gaze. She links Foucault's description of surveillance and power, "leaving the powerless at all times subject to the gaze of the powerful" (p. 32). Milstein asserts, "the zoo animal is always captive object to the human subjective gaze. The gaze is one-way, subject to object, allowing only for a one-way subject-subjective vision" ( Milstein, 2009, p. 32). The one-way gaze described by Milstein is reinforced at SeaWorld parks as spectators view captive beings, restricted in tanks and cages and powerless to the subjective gaze of humans. However, it is the documentary Blackfish that exposes and illustrates the breach in the one-way gaze where Tilikum is not subject to the gaze of the powerful but rather shifts his gaze toward the audience. This shift becomes a self-reflexive mirror where humans have their actions as captors reflected back to them via the resistance of Tilikum and others like him. His actions reflect agency and intent switching the subject position and potentially moving audiences toward coherence.

In one example of agency, the trainers agree, after watching the video of this performance, that Tilikum was aware that the food was running out because he could hear the ice clanging at the bottom of the bucket. Berg and Jett continue:

There's no food left, she kept asking him for more and more behaviors. He wasn't getting reinforced for the behaviors he was doing correctly. He was probably frustrated towards the end. Then she walked around the perimeter of G Pool. He followed her [note: ominous intense music begins to play in the film indicating he was stalking her or behaving intentionally]. And then continued over to the rocky ledge area where she laid down with him to do a relationship session, which is quiet time basically. Tilikum at some point grabbed a hold of her left forearm and started to drag her and eventually did a barrel roll and pulled her in. May have started as play, or frustration, and, uh, clearly escalated to be very violent behavior that I think was anything but play. In the end, you know, he basically just completely mutilated that poor girl ( Blackfish).

According to the autopsy report presented in the film, Brancheau's cause of death was "drowning and traumatic injuries" ( Blackfish). While Tilikum is certainly subject to the human gaze, he is not powerless underneath it but subverts it via his killing performances. Tilikum exerts power by possibly choosing when and how to act-by publicly murdering a trainer in front of the "gazing" audience.

Understanding Tilikum's attacks in this light, as a series of willful and deliberate communicative acts, is a step toward shifting our understanding of human-orca communication from implication to coherence. A coherence ideology structure requires that humans be able to recognize and understand themselves as prey or in a one-down position in order to become equal members of a biotic community. The film's overt narrative is one of power-over in that, first, humans have power over orcas by first capturing orcas and forcing them to perform for human entertainment. Second, humans have power-over in that we are responsible for driving them to psychosis and we have the power to release them, potentially situating them as passive victims without their own voice. However, the film's resistive message challenges these power-over discourses revealing power-with relationships between humans and orcas, or "knowing alongside" ( Plec, 2013) orcas. Power-with paradigms often acknowledge subaltern voices. These human-orca relationships are equal and we have to work harder to listen to, and legitimize orca communication, which might not necessarily be what we would want to hear.

Discussion: Legitimizing Subaltern More-Than-Human Communication

We claim that that the shift to coherence is one contribution to the "Blackfish Effect" and the sustained movement demanding the release of Tilikum and others like him based on prisoner-orcas legitimate communication. In the film, Christopher Porter, former Tilikum trainer, seems to have "heard" Tilikum's message and claims he understands because they had a relationship:

And you understand that he's killing, not to be a savage. He's not killing because he's just crazy. He's not killing because he doesn't know what he's doing. He's killing because he's frustrated, and he's got aggravations, and he doesn't know how to-he has no outlet for it ( Blackfish).

Porter aligns with our argument by acknowledging that Tilikum is not killing because he is "savage," "crazy," acting out of some primal predatory response, or because he is hungry. Tilikum and others like him in captivity attack and kill perhaps in an effort to be heard and to clearly communicate their disdain for their reality. We understand that we do not know what Tilikum is expressly communicating. Our intention is not to speak for Tilikum, or further continue a power-over relationship by taking the authority to read and interpret what he is "saying." However, part of making the shift to coherence is to value intuition/emotion over reason and we have scrutinized and read the film in order to interpret prisoner-orcas' symbolic meanings of material conditions. One aspect of coherence that makes this possible is empathy. Empathy is a key initial step in developing an understanding of internatural communication-it acknowledges that observation can create empathy, on one hand, while simultaneously recognizing the impossibility of complete understanding ( Plec, 2013). In this case, complete understanding need not prevent the release of prisoner-orcas. It is empathy, intuition, feeling, interconnection, and so forth that drives the shift to alternative paradigms. Witnessing often allows humans to access such shifts. As Pezzullo (2007) reminds us, "The witness is an important figure in politics because he or she can potentially take action afterward, reporting, testifying, and relating to others that which has been witnessed" (p. 146). In this way, the testimony of interviewees in the film like John Crow and John Hargrove provide a witnessing medium that contributes to a coherence frame. Simply, the acknowledgment of Tilikum as a communicating actor, allowing for his actions to be read as alternative symbolics, is enough to understand the demand for release from captivity no matter what form that freedom takes.

In an attempt to exercise our imaginary to include spaces for alternative meanings, we turn now to discussing some internatural communication possibilities. This section requires the reader to suspend some of their potential preconceived or normative views about humanature communication. One such normative view, as Callister (2013) explains in her study of human encounters with beached whales, is that there is "little room for apprehending the whale as subject capable of voice. As such, any notion of "listening" to beached whales as material rhetorical articulations is absent" (p. 47). Rather than ignore the "material rhetorical articulations" of whales, reading their bodies through internatural communication paradigms should have implications for shaping public policy. This reading of Tilikum and other attacks in Blackfish is quite literally "a rehearsal of ways of listening to non-dominant voices and non-human agents and their inclusion in the production of meaning, policy, and material conditions" ( Rogers, 1998, p. 268).

Environmental communication scholars have argued for an integrated community where humans and "extra-human citizens" participate in decision-making ( Peterson et al., 2007; Salvador and Clarke, 2011). Our article has been one attempt to illustrate how extra-human citizens participate, and even instigate, policy-making by listening to orcas as unique actors with intelligible behaviors. We push this claim despite the rhetorical tendency to write this intelligibility off as anthropocentric elitism. In this way, we employ the Weyekin principle, which holds "that in advancing an embodied critical rhetoric, the researcher attends to the corporeal experience of the non-human world so as to articulate the symbolic-material tensions obscured by predominant systems of meaning ( Salvador and Clarke, 2011, p. 248). In understanding and listening to captive orcas, both at SeaWorld and other marine prisons, we may begin to see them as a crucial part of the "Blackfish Effect," the policy proposals, and SeaWorld boycotts that have followed. In this way, orcas create a form of protest rhetoric that has observable implications on policy reform. Rather than dismiss Tilikum as a malleable part of nature used for human anthropocentric ends, we should acknowledge Tilikum as the first actor, the deliberate catalyst, for the effect. Tilikum, and the other orcas stories discussed in Blackfish, were the first activists that initiated this particular environmental justice movement.

Reading the whales-as-activists takes us to another potential understanding of captive orcas. As previously discussed, the prisoner metaphor is important in challenging the normative narrative of captivity as important for "environmental education and science," as claimed by SeaWorld. But the prisoner-orca metaphor can go further in highlighting the whales' agency. We suggest, instead, the political prisoner metaphor. Captive orcas are not simply held captive. Rather, they are activists imprisoned for political reasons, for example, animal exploitation for corporate profit. Their deliberate actions while in captivity may be meant to communicate a political injustice to their "free" audiences. Milstein (2011) coins the term "whale insiders," to refer to researchers, advocates, and others who may become advocates for preservation based on a direct nature experience with whales in the wild ( Milstein, 2011, p. 7). Viewers of Blackfish may not have direct experience with wales in the wild but are exposed to the film's narrative of captivity preventing a wildlife. To this end, Milstein (2011) discusses how wild "whale insiders" see the potential relationship between orcas in the wild and captive orcas, understanding "the first captive orcas as, in a sense, serving as ambassadors for wild orcas" (p. 8). Tilikum may certainly be an ambassador for wild orcas, and in this instance, he may be a political prisoner-orca demanding an end to capture and captivity as it is practiced throughout the world. This highlights "the need to [not only] listen to the other-than-human, but to treat them as agents, as active participants in the construction of meaning" ( Schutten and Rogers, 2011, p. 274).

Alternative symbolics, and by extension alternative listening abilities, requires practice in expanding our perceptions. In this way, Blackfish has provided audiences with a boundary breach that has led to the "Blackfish Effect," which can be interpreted through frames of internatural communication. Importantly Carbaugh (2007) outlines "Touchstones on Earth" and charges the reader with a challenge stating that we need to "open our understanding to the world beyond our words, beyond our representations of it, to learn anew from it, and to be in a position better to speak about what we come to know and thus to act accordingly" (p. 68). By telling Tilikum's story and other prisoner-orca narratives, the film has illustrated complicity and implication, and, finally, allows for expansion of meaning toward what a coherence lens might include. Coherence necessitates that audiences take orca communication seriously and acknowledge them as key players in shaping public policy and participating in environmental social movements. Utilizing Plec's (2013) three categories and, in particular, expansion of a coherence framework, helps take our interpretation of Blackfish deeper to incorporate orca communication into our understandings of environmental social movements and answering Carbaugh's challenge. Furthermore, this framework complicates our understandings of the binary as it is symbolically arrogant and materially impossible. This prescriptive framework, applying complicity, implication, and coherence, could be seen as a guide for environmentalists as they work to incorporate internatural communication into understandings of captivity and sustainability practices. If the political prisoner metaphor is taken into consideration and, we contend, moves beyond metaphor, it would be within the realm of possibility for captive orcas to work alongside human political activists to campaign for a Presidential pardon. In the campaign for orca justice, we can hope "that in 50 years we'll look back and think, 'My God, what a barbaric time" ( Blackfish).

Author Notes

We would like to thank the reviewers for their extremely helpful comments toward developing our essay. We also thank Dr. Connie Bullis for her insightful guidance with an earlier draft. An earlier version of this essay was presented at the Conference on Communication and Environment in Boulder, Colorado in June 2015 and we thank those who gave us great feedback after our presentation. Finally, we thank Tilikum for initiating anti-captivity movements around the globe.

Author Contributions

Both authors researched, wrote, revised, and came up with the intellectual content for this essay equally.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

McHendry, G. (2012). Whale Wars and the axiomatization of image events on the public screen. Environ. Commun. 6, 139-155. doi:10.1080/17524032.2012.662163

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Internatural Activists and the "Blackfish Effect": Contemplating Captive Orcas' Protest Rhetoric through a Coherence Frame

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The documentary film Blackfish (2013; www.blackfishmovie.com) follows Tilikum, a captive SeaWorld prisoner-orca responsible for the death of trainer Dawn Brancheau and two others. The film has had a profound effect on public perceptions of orca captivity creating the "Blackfish Effect." Our critical analysis of the film engages Plec's (2013) internatural communication categories of complicity, implication, and coherence.

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Legislation such as the Species at Risk Act protects orcas. There are also efforts to gather scientific data about the species as well as cooperate with other countries such as the U.S. to protect orcas in all waters.

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Orcas hunting

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Orca population distribution

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Two forms of killer whales, the "resident" form and "transient" form, have been distinguished British Columbia and Washington State (Bigg, 1982; Bigg et al., 1990). While many researchers currently recognize that the terms resident and transient whales are somewhat misleading in their descriptions, the terms are still so entrenched in the popular and scientific literature that they continue to be used.

The two sympatric (living in the same area) forms are believed to differ in several aspects of morphology, ecology, and behaviour. However, much of what we know about the resident and transient form and/or behaviour of killer whales is derived from research conducted in the northeastern Pacific and then extrapolated to other areas.

It is possible that killer whales occupying other geographical regions or habitats (e.g., offshore environments) may behave and/or segregate differently. Bigg et al. (1987), based on observational data only, noted that the dorsal fin of resident whales tended to be more rounded than those of transient whales. Baird and Stacey (1988) documented differences in saddle patch pigmentation. Bigg et al. (1987) stated that resident pods range in size from 5 to 50 individuals and transient pods range from 1 to 7.

Resident pods are believed to have smaller home ranges than transient whales; however, little is known regarding killer whale winter range and distribution.

Differences have been also noted in the vocalization patterns between the two forms (Ford, 1989; Ford and Hubbard-Morton, 1990).

Northeastern Pacific resident killer whales are mainly piscivorous and rarely prey on marine mammals.

Transient whales frequently are seen pursuing marine mammal prey, but there are cases of transient whales eating both fish and marine mammals in southeastern Alaska (M. Dahlheim, personal observations) and Prince William Sound, Alaska (Matkin and Saulitis, 1994).

Studies on mDNA restriction patterns provide evidence that the resident and transient pods are genetically distinct (Stevens et al., 1989; Hoelzel, 1991a; Hoelzel and Dover, 1991).

Killer whales usually occur in small pods, with typically fewer than 40 individuals. Large groups may reflect the temporary merging of a number of pods, possibly related to seasonal peaks in prey availability or reproductive activities. Single whales, usually adult males, occur infrequently (Norris and Prescott, 1961).

Bigg et al. (1990) examined the social organization and genealogy of resident killer whales in the coastal waters of British Columbia and Washington State. The authors classified the social organization into communities, pods, subpods, and matrilineal groups. They defined these terms as follows:

a community is composed of individuals that share a common range and are associated with one another;

a pod is a group of individuals within a community that travel together the majority of time;

a subpod is a group of individuals that temporarily fragments from its pod to travel separately; and

a matrilineal group consists of individuals within a subpod that travel in very close proximity.

Matrilineal groups are the basic unit of social organization, and consist of whales from 2-3 generations.

Occasionally, when resident pods encounter each other after being separated for some time, the pods will form two tight lines and approach each other head on. When the groups are within 10-20 m of each other, they stop motionless at the surface and hover, facing each other for 10-30 sec (Osborne, 1986). Intermingling typically follows this greeting ceremony. Intermingling is characterized by slow moving and tight milling concentrations of whales. Many of the whales are in physical contact, rolling and brushing against each other at or near the surface.

Parallel scars caused by the tooth marks of other killer whales indicate that some intraspecific aggression occurs (Greenwood et al., 1974). However, parallel scars could be obtained during other social activities. Many scratches or rake marks may also be the result of interactions with pinnipeds during predation events (M. Dahlheim, personal observations).

Care-giving is well documented (Caldwell and Caldwell, 1966). Waite (1988) describes alloparental care in killer whales. Adolescent females performed most of the alloparenting, although non-reproductive females and males were also observed to alloparent. Adult bulls have been observed to "baby-sit" groups of calves and juveniles (Osborne et al., 1988).

Although regular sightings and recurrence of the same pods have been documented within specific areas, territoriality among pods has not been documented.

Transient whales appear to cover a more extensive range than residents. A distance of over 2600 km (California to Alaska) has been reported for a transient group (Goley and Straley, 1994).

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Two forms of killer whales, the "resident" form and "transient" form, have been distinguished British Columbia and Washington State (Bigg, 1982; Bigg et al., 1990). While many researchers currently recognize that the terms resident and transient whales are somewhat misleading in their descriptions, the terms are still so entrenched in the popular and scientific literature that they continue to be used.

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About a decade ago a SeaWorld trainer was killed by an orca. A lot of people viewed these animals as dangerous.

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Dawn Brancheau died at the tourist attraction in Orlando, Florida, on February 24, 2010 - exactly a decade ago - after Tilikum, a captive whale dragged her underwater and thrashed her around a pool. The 40-year-old suffered fractures to her jaw, several ribs and part of her vertebra in the tragic incident witnessed by terrified onlookers. An autopsy released a month after her death detailed how the experienced trainer died of blunt force trauma to the head, neck and torso, and drowning.

In a statement released on Monday, a spokesperson for SeaWorld said: "Today, the entire SeaWorld family remembers and honors the life of Dawn Brancheau and her passion for protecting all animals, and inspiring the next generation to care for our oceans and its marine animal inhabitants."

After petting the whale on the nose during a show, she turned her back before the orca pounced.

He yanked her into the pool and began violently thrashing her around.

While some members of staff quickly herded visitors out of the pool area, others rushed to try to free their colleague from the beast's grip.

But sadly, by the time Dawn's body was retrieved she had already died.

Her scalp was found at the bottom of the pool after SeaWorld staff managed to guide Tilikum into an adjoining area.

Dawn had studied psychology and animal behaviours at university and was one of SeaWorld's most celebrated trainers.

Former colleagues said the trainer's bond with Tilikum was strong and based on trust.
READ MORE: SeaWorld announces death of baby beluga whale
Dawn had spent 15 years working with sea creatures, many of them deadly.

She became a trainer of the killer whales two-years after she started working at Seaworld.

Tilikum, also known as Blackfish, was among the largest fish at SeaWorld.

The bull orca measured 22.5 feet in length and weighed about 12,500 pounds.
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He was captured in a net near Iceland in 1983 at just two years old.

He spent his first year in captivity living in a tank at a marine zoo in Iceland.

After this stint, he was shipped to Sealand of the Pacific, a marine park on Vancouver Island in British Colombia.

Here he had to perform in eight shows every day for visitors.

He killed a 21-year-old trainer in 1991 at the site shortly before it was closed.

After being transferred to SeaWorld he was found to have killed a 27-year-old man who evaded security to ender an orca tank.

Dawn was Tilikum's third victim.

SeaWorld of Hurt, a campaign group which raises awareness about the realities faced by the captured whales in SeaWorld, calls the US site a "prison".

Activists have called for the tourist attraction to be closed as whales, dolphins and other big fish cannot live in their natural habitat.

SeaWorld declined to comment on the allegations.

Last summer, American Humane, a non-profit which works to promote animal welfare, praised SeaWorld's "exceptional standards".

Paul Boyle, national director of Animal Humane, said: "Animals need and deserve great welfare, and families deserve to know that the zoos and aquariums they visit are doing right by the animals in their care.

"American Humane has recognized SeaWorld as having exceptional standards for the humane treatment of the tens of thousands of animals in its care and the thousands they have rescued, nursed back to health, and released.

"Our organization, the country's first national humane organization and the world's largest certifier of animal welfare, certified SeaWorld's parks last year in San Antonio, San Diego, and Orlando, as well as Busch Gardens Tampa Bay, through our Humane Certified program.

"The parks passed rigorous and lengthy third-party animal welfare audits, earning this prestigious certification."

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SeaWorld tragedy: Orca killed experienced trainer leaving her with horrific injuries

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Dawn Brancheau died at the tourist attraction in Orlando, Florida, on February 24, 2010 - exactly a decade ago - after Tilikum, a captive whale dragged her underwater and thrashed her around a pool. The 40-year-old suffered fractures to her jaw, several ribs and part of her vertebra in the tragic incident witnessed by terrified onlookers.

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While SeaWorld has ended their breeding program, China has begun to pick up this practice.

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SeaWorld announced a year ago that it would end orca breeding at its parks in the U.S. One year later and nearly 8,000 miles away in China, another such program is just getting started.

The Chimelong Group, one of the country's biggest amusement park operators, revealed that it opened a breeding center for orcas on February 24 at Chimelong Ocean Kingdom-the first program of its kind in China. Located in Zhukai, a city in the southeast, the park has five males and four females ranging in age from five to 13. The orcas, also known as killer whales, were plucked from Russia's Sea of Okhotsk, according to the China Cetacean Alliance, a coalition of international conservation organizations.

On its website, the company says it aims to "raise public awareness about killer whales and their conservation status" and "conduct research." It adds that it plans to build a marine science museum where the orcas will be displayed. It will also work with other facilities to "promote the breeding of killer whales."

It's unclear whether the orcas will perform. Nonetheless, concern by conservation groups in China over their welfare, as well as the prospect of other parks opening breeding centers, has mounted since the Chimelong announcement. The park hasn't responded to a request for an interview.

Shifting Away From Captive Orcas

Orcas are the largest dolphin species and one of the smartest predators in the world. Scientists say that the lack of stimulation and cramped, unnatural conditions in captivity can stress them out, manifesting in stereotypic behavior such as biting and swimming in circles repeatedly. Whales and dolphins die much younger in captivity than in the wild, according to Whale and Dolphin Conservation, a U.S.-based charity dedicated to the animals' protection.

But unease over the well-being of the orcas at Chimelong extends beyond these broad concerns.

For one thing, the orcas could be family because they were captured from the same habitat in Russia, says Taison Chang, chairman of the Hong Kong Dolphin Conservation Society, a nonprofit devoted to the protection of cetaceans-meaning dolphins, whales, and porpoises. "If they're related, sooner or later they'll find some genetic diseases in the orcas because they'll keep inbreeding," he says.

Their diet could also pose a problem, according to Chang. Employees feed them fish, the Chimelong Group says, but researchers believe that wild orcas in the Sea of Okhotsk eat only mammals such as seals and sea lions. And the male-skewed sex ratio may lead to destructive aggression, he says, given that male orcas are naturally feisty and may fight to win a mate.

"I will be personally astonished if these animals successfully breed," says Naomi Rose, a marine mammal scientist with the U.S.-based Animal Welfare Institute.

Growing awareness about the problems associated with captive cetaceans have led marine parks around the world to shut down or redefine themselves. In recent years a handful of countries, including India and Switzerland, have banned the keeping of orcas in captivity.

Public scrutiny intensified after the 2013 release of the documentary Blackfish, which cast a critical eye on the marine entertainment industry. SeaWorld, one of the best known marine parks, ended orca breeding and some of its shows in 2016, after years of declining ticket sales and decreased profits. (Read more about SeaWorld's decision to end orca shows and breeding.)

"Changing the tanks or the style of show is not going to meaningfully relieve the animals of suffering," said Jared Goodman, PETA Foundation's director of animal law, in a statement after SeaWorld's announcement last year. "The movie Blackfish was the beginning of the end for the practice."

A Burgeoning Industry

China appears to be immune to the "Blackfish effect," the term often used to describe the public's response to the film. In fact the country's marine park industry is booming, with 44 facilities today, up from 39 in 2015, according to the China Cetacean Alliance. Nineteen more are scheduled to open in the next two years.

Chang thinks Chimelong has paved the way for more orca breeding in China. "The facilities in China will be like a photocopier machine," he says.

According to Chang, two other parks-Shanghai Haichang Polar Ocean Park and Linyi Polar Ocean Park-plan to import, or have already imported, orcas from Russia, which sets a yearly quota for the number of orcas that can be taken from the wild. This year, it's 10. (The practice of taking orcas from Russian waters is controversial because little is known about their numbers. "You can't determine a sustainable number if you can't determine a population to start with," Rose explains.)

China's marine park industry got started only about ten years ago, Chang says, whereas people in the West have been familiar with marine entertainment for decades. "Today a lot of Chinese people are still very interested in the whole idea of seeing animals in captivity," he says.

Other Asian countries, notably Japan, also boast marine parks, but Chang says China stands out as the only nation that's expanding the business at such an aggressive rate.

In addition to ocean theme parks, shopping malls, restaurants, and other unorthodox venues increasingly feature bears, walruses, and other wildlife to attract customers. A polar bear named Pizza gained international attention in November 2016 after video surfaced of him pacing and pawing at a vent in a barren enclosure at a Chinese mall.

China has no federal animal welfare laws, and amendments to the country's primary conservation law specifically allow animal performances at privately owned safari parks, marine parks, aquariums, and circuses.

But Peter Li, Humane Society International's China expert, previously told National Geographic that there's a growing awareness among China's young about animal welfare. And groups like Chang's hope to hold facilities accountable through investigations and public awareness efforts. Chang says he doesn't want to put parks out of business, but he does want them to consider other ways of educating the public about whales and dolphins.

That's an idea whose time has come- new technology is already allowing people to witness the splash of a virtual whale just feet from where they stand.

Read more stories about wildlife crime and exploitation on Wildlife Watch. Send tips, feedback, and story ideas tongwildlife@natgeo.com.

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China's First Orca Breeding Center Sparks Controversy

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SeaWorld announced a year ago that it would end orca breeding at its parks in the U.S. One year later and nearly 8,000 miles away in China, another such program is just getting started.

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The Navy will stop polluting waters off the coast of Washington, which has endangered orcas.

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The U.S. Navy has signed a court order requiring that it stop scraping hulls of decommissioned ships in a way that discharges contaminants into Sinclair Inlet near Bremerton.

As state senators celebrated Navy Day at the Legislature in Olympia, the Navy was agreeing in federal court that it will embark on a project to reverse environmental damage caused by scraping decades of marine gunk off the hulls of ships.

"The Navy's reckless actions endangered Washington's diverse marine life including salmon and orcas: Everyone has a duty to protect our waters, including the federal government," Attorney General Bob Ferguson said in a statement. Ferguson was under the weather and unable to attend a celebratory briefing.

The settlement came after the Navy was sued in U.S. District Court by the Suquamish Tribe, the Puget Soundkeeper Alliance, a lawsuit joined last year by the Washington Attorney General's office. It was Ferguson's 55th lawsuit against the federal government since the Trump Administration took office, and the AG's 25th victory.

The suit arose out of a 2017 effort by the Navy to blast marine debris off the decommissioned 60,000-ton aircraft carrier U.S.S. Independence before it was sent to Texas to be scraped. The Navy dumped 73 truckloads of gunk into Puget Sound. Metals from the carrier's anti-fouling hull paint included copper and zinc.
RELATED: Congress to Navy: Monitor, report noise from Growler jets over Whidbey Island
Under a consent decree, the Navy has agreed to stop water scraping for a full decade. During the 10-year moratorium, the Navy must use a drydock to clean inactive ships, thus keeping materials out of Puget Sound.

The lawsuit settlement won praise from Leonard Forman, chairman of the Suquamish Tribe, who described it as "a step toward repairing the tribe's and Navy's government-to-government relations" as well as serving to "protect treaty reserved waters."

The Independence was decommissioned in 1998. The Navy's scraping yielded pollutants substantially in excess of amounts permitted by the U.S. Environmental Protection Agency and the state Department of Ecology.

According to an old joke, if the Navy had one more installation along the shores of Puget Sound, the shoreline would sink.

The Navy repairs ships at the Puget Sound Naval Shipyard. It sends one of America's most lethal weapons to sea at the Trident submarine base on Hood Canal. Navy Base Keyport is used for the manufacturing, testing and development of undersea warfare systems.
RELATED: Attorney General Bob Ferguson sues Trump Administration: Put courthouse immigration arrests on ice
A Navy carrier base is located on Port Gardner Bay in Everett, while Naval Station Whidbey trains pilots and is expanding with arrival of 36 more Growler jets.

Symbolized by the "Sound of Freedom" sign on U.S. 20, just north of Oak Harbor, the Navy has pushed aside local protests on grounds that its facilities are vital to its national defense mission. AG Ferguson has taken it on twice, with litigation over the shipyard's scraping of the Independence and noise caused by the Growler jets on central Whidbey Island.

Hence, settlement of the scraping case is unusual.

As Katelyn Kinn, attorney for Puget Soundkeeper, put it: "This settlement demonstrates that no entity in this country, regardless of how big and powerful, is above the laws in place to protect our precious waters and communities that rely on them."

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Navy will stop scraping ship hulls and polluting Puget Sound

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The U.S. Navy has signed a court order requiring that it stop scraping hulls of decommissioned ships in a way that discharges contaminants into Sinclair Inlet near Bremerton. As state senators celebrated Navy Day at the Legislature in Olympia, the Navy was agreeing in federal court that it will embark on a project to reverse environmental damage caused by scraping decades of marine gunk off the hulls of ships.

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Breeding orcas at SeaWorld (before they stopped)

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Our current practices have to be evaluated to determine what actions to protect the orcas we must prioritize.

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Introduction

Conservation science is tasked with quantifying the relative importance of multiple anthropogenic threats to species, both to determine if cumulative impacts exceed sustainable levels and to guide effective recovery plans1,2,3,4. However, cumulative human impacts are often poorly understood and inadequately addressed in conservation and management5. Fundamental research is still needed to integrate information on qualitatively different stressors into comprehensive models that reveal the cumulative impacts on measures of population growth, stability, and resilience6. Such work is needed, in part, because threats vary widely in their amenity to mitigation. When regulators require users to forego economic opportunities, it is important to have confidence that management actions will achieve the desired effect7. One way to accomplish this is to conduct "population viability analyses" (PVA) that use models of population dynamics to evaluate the relative importance of multiple anthropogenic stressors, singly and in combination, so that conservation can be directed toward efforts most likely to promote species recovery8. PVA can be a powerful tool for informing management and conservation decisions. However, the detailed population models used in PVA depend on: availability of estimates for demographic rates (both fecundity and survival and the variability in such rates); confidence that observed past rates are predictors of ongoing demography, or that trends can be foreseen; data for quantifying effects of threats on demographic rates; and a population model that adequately captures the key demographic, social, genetic, and environmental processes that drive the dynamics of the population of concern. Nevertheless, even when data on certain aspects of the population or its threats are not available, we can use PVA models to explore possible outcomes across a plausible range of values, and thereby identify which factors might be important and the target of additional research.

The Southern Resident killer whale ( Orcinus orca, SRKW) population in the northeastern Pacific Ocean is one of the most critically endangered populations of marine mammals in the USA9 and Canada10. The USA and Canada have listed this transboundary population as Endangered, citing three primary risk factors: lack of the whales' preferred prey, Chinook salmon ( Oncorhynchus tshawytscha); chronic and acute underwater noise and physical disturbance (e.g., from ferries, commercial ships, whale-watching boats, fishing boats, and recreational traffic); and high levels of contaminants, including polychlorinated biphenyls (PCBs)10,11. A recent Status Review12 highlighted also the potential risk to this small, localized population from catastrophic events such as an oil spill. Governments and non-governmental organizations are currently seeking effective conservation measures for this high-profile population. Fortunately, the biological and environmental data available for SRKWs are rich by the standards of any marine mammal population. Long-term annual censuses, with continuous monitoring since 1976, coupled with the specialized diet, have allowed inference of quantitative relationships between prey and various metrics of fecundity and survival13,14. Thus, the prerequisites for a robust PVA suitable for guiding conservation are met.

PVA uses demographic models to assess risk to wildlife populations and evaluate the likely efficacy of protection measures, recovery targets, and restoration options15,16. We used the Vortex PVA model to examine the dynamics of SRKWs. Vortex17,18,19 is a flexible, individual-based simulation that is freely available. Vortex has been used to set recovery goals and guide actions for many threatened species, including the Mexican wolf ( Canis lupus baileyi)20, Florida panther ( Puma concolor coryi)21, and Florida manatee ( Trichechus manatus latirostris)22. Several recent PVAs on the SRKWs have shown how variability in demography23 or inter annual variability in Chinook salmon abundance12,24,25 could affect the population. We extend those approaches to consider also the sub-lethal effects of contaminants and acoustic disturbance, and the cumulative impacts of threats and interactions among them.

We first parameterized a Baseline model with demographic rates observed over 1976 through 2014, and tested the sensitivity of population growth to each demographic parameter. We then constructed one model that quantifies the population consequences of all three anthropogenic threats to SRKWs identified in Canadian10 and USA11 recovery plans. We compared the relative importance of each threat by projecting the population growth across the possible range of each threat. Finally, we used the PVA to explore the degree to which threats would have to be mitigated, alone or in combination, to reach a quantitative USA recovery target of sustained 2.3% growth over 28 years11.

Results

Five sets of population models and the scenarios examined in each are listed in Table 1. The Baseline model projects mean population growth over the next 100 years of r = −0.002, with variation across years of SD = 0.045 (Fig. 1). These projections match very closely to the rate of r = 0.002, with SD = 0.042, observed over 1976 to 2014. The marginally lower growth in the model can be accounted for by future accumulation of low levels of inbreeding. After 100 years, the projected mean inbreeding coefficient is 0.067, about the same as results from mating between first-cousins. When inbreeding depression was eliminated from the Baseline model, the projected growth was r = 0.002, with SD = 0.043 - nearly identical growth and variation in growth to the trend in recent decades, and thereby confirming that the model replicates accurately the recent dynamics of the population.

Table 1 Models of viability of the SRKW population for assessing current viability, sensitivity to anthropogenic threats, and responses to management.

Sensitivity tests of the influence of each demographic rate in the baseline PVA (Supplementary Information) show that, across the ranges of values tested, variation in fecundity (defined for the model as the mean proportion of adult females giving birth per year) accounts for most (77%) of the uncertainty in population growth rate. Annual adult mortality has some influence on the population trajectories (6%), but because mortality is already close to 0, there is comparatively less opportunity to improve the value of this parameter. Calf (first year) and juvenile (1 y to 10 y) mortality each accounted for about 3% of variation in population growth. Individual variation in reproductive success and temporal fluctuations (EV) in demographic rates had almost no effect on long-term population growth, as would be expected for a very long-lived species in which short-term fluctuations average out over time. Therefore, although our estimates of annual variation in rates are uncertain, refining the estimates would not change any conclusions about the effects of threats on the viability of the population. Given the small population size, inbreeding depression might cause sufficient adverse impact on population viability (6% of the total variance explained) such that it should not be ignored in assessments of long-term population viability. The impact of inbreeding was exacerbated slightly when we did not include avoidance of very close inbreeding (Supplemental Information).

Individual Threats

The set of models that includes estimates for the threats identified in the recovery plans - Chinook prey availability, noise and disturbance, and contaminants - was calibrated so that in the Current Threats scenario the demographic rates at existing threat levels reflect the mean demographic rates observed from 1976 through 2014. Thus, the Current Threats scenario mirrored the simpler Baseline scenario, except that rounding error in estimating effects of threats led to very slight deviation from the Baseline. The levels of these threats were then varied across broad ranges of values to determine which threat would have the greatest impact on population growth. Over the ranges tested, the effects of Chinook prey abundance on fecundity and survival had a greater effect on the population growth rate than did the other two factors (Fig. 2). Noise disturbance acts through decreased feeding efficiency in our model, but has a lesser effect than prey abundance because the maximum impact of boat noise 100% of the time would be to reduce foraging by about 20%. PCB accumulation rates that we tested result in mean levels in adult females of 0 to 132 ppm. Across this range, calf mortality is predicted to rise from about 7% to 50% (see Methods), and this impact shifts population growth from slightly positive to negative.

Cumulative Threats

Threats may interact, such that cumulative effects differ from those projected based on the summation of individual impacts. Full exploration of all of the possible interactions among the threats to the SRKW is not warranted at this time because individual threats are not yet well quantified. As more data on the above threats and other threats are acquired, management authorities can use the PVA framework to examine specific interactions of interest or full statistical analysis of all possible interactions26. To illustrate how cumulative threats can be assessed within the PVA model, we examined combinations of threat levels that represent the cumulative impacts of multiple threats for a few sample scenarios. We compared the Current Threats to a scenario with no anthropogenic threats and to scenarios with an increase in current threats and the addition of new threats. Figure 3 compares the population trajectory for the Current Threats with a scenario in which noise and PCB contamination were set to 0, and with two scenarios that describe levels of threat that could occur with proposed further industrial development and climate change. Table 2 shows the mean growth rates, probabilities of decline below 30 animals, and probabilities of extinction within 100 years under these scenarios.

Table 2 Measures of viability of the SRKW population over 100 years under scenarios of minimal anthropogenic threats, current threats, and two levels of increased threats due to development.

The population could show robust growth if all anthropogenic threats were removed, but has no growth under current threat levels (Fig. 3). The combination of increased and additional threats expected under planned further industrial development in the habitat of the SRKW would cause population decline.

Demographic Management

The potential benefits of improvements in the primary demographic rates were examined in a set of Demographic Management scenarios. The demographic analyses indicate that reaching the SRKW recovery target of 2.3% growth is impossible by improving any single rate by a plausible amount, although increased fecundity would have the greatest positive influence on population growth (Fig. 4). To reach the recovery target, sustained mitigation of threats will be necessary to promote both increased fecundity and reduced mortality.

Threat Management

Improvements in demographic rates would need to be achieved by management actions that reduce threats or otherwise enhance the environment for SRKW. We therefore examined how population growth would respond to reductions in the levels of current threats. To achieve the recovery goal by increasing Chinook abundance alone would require a return to nearly the highest rates of Chinook abundance observed since 1979 (Fig. 5). If eliminating acoustic disturbance while maintaining current levels of Chinook abundance were possible, annual population growth could reach 1.7%. Removal of PCBs from the habitat would result in marginally positive (0.3%) growth, but the effect is much smaller than the impact of reduced noise and disturbance or increased Chinook abundance. Complete removal of both acoustic disturbance and PCBs is predicted to result in 1.9% growth. Therefore, reaching the recovery target without increasing Chinook salmon numbers is likely impossible. Reducing acoustic disturbance by 50% and simultaneously increasing Chinook by more than 1.15x would allow the population to reach the 2.3% growth target. Other combinations of mitigation should be explored by management authorities as conservation options are identified.

Discussion

The SRKW population has experienced almost no population growth during the past four decades, and it declined in the last two decades. Intensive monitoring of the population since 1976 provides the information for construction of a detailed PVA model that closely replicates the observed population dynamics, and thereby provides a basis for projections under scenarios of increased anthropogenic threats or, conversely, increased mitigation actions. Models projecting population changes based on average demographic rates and fluctuations in those rates project that under the status quo the population will most likely remain near its current size. However, our use of baseline demographic rates averaged across 38 years of monitoring might give an overly optimistic projection for the SRKW if rates have deteriorated in recent years. A population projection based on demographic rates observed through 2011 projected a 1% annual mean growth25, but a recent Status Review12 projects a decline of 0.65% per year if demographic rates (such as recently lower fecundity) remain as they have been during 2011-2016. If ongoing monitoring indicates that these are not just short-term fluctuations in rates, then assessments of current viability, vulnerability to new or increased threats, and measures needed to achieve recovery will need to be revised.

When examined over ranges that encompass plausible improvements, the demographic parameter that presents the better opportunity for a large benefit to population growth is fecundity, rather than mortality. This finding is similar to a study of two bottlenose dolphin ( Tursiops aduncus) populations off Australia, which found that variability in reproduction was more important than variability in mortality in driving differences between the populations27. There is simply more potential for improving reproduction than for improving adult survival when survival is already close to 1. Even complete elimination of adult mortality in the SRKW (not a biological possibility) would result in a population growth rate of 1.8%, still below the recovery goal of 2.3% growth. Although recovery cannot be achieved solely by improving adult survival, any decline in adult survival caused by new or exacerbated threats could have serious consequences for the population.

The PVA was useful for exploring scenarios representing the three main anthropogenic threats - prey limitation, acoustic and physical disturbance, and PCBs - that might worsen with increased development, or could be mitigated through management. Across the ranges of threat levels that we examined, reduction of the prey base was the single factor projected to have the largest effect on depressing population size and possibly leading to extinction, although either higher levels of noise and disturbance or higher levels of PCB contamination are sufficient to push the population from slow positive growth into decline. If additional threats from proposed and approved shipping developments (such as catastrophic and chronic oil spills, ship strikes, and increased vessel noise) combine with the predicted decline of Chinook due to climate change28, then the population could decline by as much as 1.7% annually, have a 70% probability of declining to fewer than 30 animals, and have a 25% chance of complete extirpation within 100 years.

Mitigating multiple anthropogenic threats sufficiently to reach the recovery target will be difficult. The PVA is a useful way for managers to identify priorities for future research, and to focus conversations with ocean users and other special interests about the most pragmatic ways to promote recovery of endangered species. Those discussions must be integrated with considerations of feasibility, cost, societal impact, and timeframe for effective implementation. If a threat cannot be mitigated in a timescale relevant to conservation, or if costs are so high that they are prohibitive, thinking of those intractable problems as "fixed costs" in a cumulative impact management framework4 might be useful. For example, our model results show that eliminating PCBs would provide less benefit to SRKWs than improving salmon returns or reducing anthropogenic noise and disturbance. This is fortuitous because imagining a way to eliminate PCBs that are persistent in the ecosystem is problematic29, even though levels in tissues of SRKWs have been slowly declining in recent decades30. Identifying fixed costs that are difficult or impossible to mitigate allows a practical discussion about how to rank recovery actions among the anthropogenic factors that can be managed.

Of the three threats we considered, across wide but plausible ranges of each, salmon abundance is the greatest factor affecting SRKW population dynamics. Previously reported correlations of demographic rates with Chinook abundance13,14,24 were used to parameterize our model, and Wasser et al.31 recently offered insights into a mechanism that could cause the effect on fecundity: hormone levels indicate that SRKWs experience nutritional stress related to periods of lower abundance of Chinook prey and that this stress results in fewer successful pregnancies. Our PVA model estimated that SRKW recovery cannot be achieved without reaching the highest levels of salmon abundance observed since 1979, which was 30% higher Chinook salmon abundance than the long-term average between 1979 and 2008. This model result allows managers to focus discussions on whether achieving such a high sustained level of salmon abundance is attainable, and if so, how to achieve it. For example, removal of a hydroelectric dam on the Elwha River in the state of Washington is expected to increase spawning habitat for all five wild Pacific salmon species in the Salish Sea, but discussions about dam removal began in the 1960s32 and the cost was in the hundreds of millions of US dollars. Restoration of spawning and rearing habitat could improve growth and survival of wild, juvenile salmon, but this takes political will, time, and money33. Improvement of marine survival of juvenile salmon might be possible by better management of net-pen salmon aquaculture sites that host and amplify viruses and parasites that have the potential to reduce survival of wild salmon34,35. Reducing Chinook harvest could provide an interim and strategic opportunity to rebuild depressed wild Chinook salmon runs and increase the number of Chinook available to whales in terminal areas like the Salish Sea36. Harvest reductions without longer term rebuilding plans might be an incomplete measure in places where Chinook harvests are already low due to abundance concerns or other constraints37.

The SRKW population could be adversely affected by any new threats and further intensified impacts of the anthropogenic threats that we did assess. For example, pollutants other than PCBs might affect the population, and PCBs are known to have adverse effects beyond just reduced infant survival - such as reduced immune function38. However, other than calf survival, sufficient data are not yet available on the impacts of PCBs on demographic rates to allow incorporation of those threats in the population model. Moreover, threats to the population likely interact, perhaps in non-linear ways. For example, cetaceans that are food-limited might mobilize more lipids, and this will change the accumulated loads and harmful effects of PCBs and other organic pollutants. Similarly, reduction in foraging success because of boat noise might be of little consequence if prey is abundant, but could be critical if killer whales have difficulty procuring enough prey. If we can obtain data on additional threats and the interactions among threats, such effects could be included in the PVA models. At present, given that only estimates of approximate average effects of some threats are included in the model, inclusion of higher level interactions is premature.

While acknowledging that we examined only the identified primary threats to the SRKWs and that we cannot yet fully assess possible complex interactions among those threats, an important finding from our PVA is that reaching the recovery target will likely require mitigation of multiple threats. For example, the PVA projects that a 50% noise reduction plus a 15% increase in Chinook would allow the population to reach the 2.3% growth target. Noise is a particularly attractive issue to address in a management context, because it is amenable to several possible mitigation scenarios39,40. With respect to noise from commercial shipping, preliminary calculations suggest that the distribution of source levels of individual ships follows a power law, implying that quieting the noisiest ships will reduce overall noise levels by a disproportionate amount41. Identifying the noisiest ships operating in SRKW critical habitat42 and creating incentives to reduce their noise outputs through speed restrictions and maintenance might generate considerable reductions in noise levels. The International Maritime Organization and the International Whaling Commission have urged nations to reduce the contribution of shipping to ocean ambient noise, with some countries adopting a pledge to reduce anthropogenic noise levels by 50% in the next decade43. However, from the perspective of a foraging killer whale that emits high-frequency (18-32 kHz) echolocation clicks to detect and capture salmon, high-frequency noise from small, outboard vessels that follow whales might cause a greater reduction in a killer whale's foraging success than low-frequency (<1 kHz) background noise from commercial shipping44.

Clearly, even without new or increased external threats, the SRKW population has no scope to withstand additional pressures. The current situation for SRKWs gives little cause for optimism. This is likely to worsen, given the energy-related project proposals already approved for the region45, which will increase broadband ocean noise levels and the risk of ship strikes and oil spills46. Our models of the additional threats expected with a proposed increase in oil shipping show that these threats will push a fragile population into steady decline. Obviously, countering such additional threats sufficiently to achieve SRKW population recovery would require even more aggressive mitigation actions than if there were no such increasing threats to the population.

The case study we present offers an unusual opportunity to examine multiple anthropogenic threats in a wildlife population that is extremely data-rich by the standard of any marine ecology study5. One threat (the impact of prey abundance through the prey-demography link) has been well studied for decades. Another (acoustic disturbance) is relatively well appreciated in that there are documented relationships between higher noise level and reduction in foraging success. However, a conceptual step is required to convert the reduction in foraging to a reduction in prey acquisition. Full consideration of noise impacts would need to include complex interactions among reduced foraging time, reduced detection space, and reductions in prey availability. The third kind of threat (population consequences of PCBs and other persistent pollutants) relies on very few data points to calibrate the effect of the PCBs only on whale calf survival, which underestimates the total population consequences of contaminants in two ways. Lack of concentration-response studies on compounds other than PCBs hinder our ability to model population consequences of PBDEs or other contaminants. Similarly, existing studies do not allow us to predict effects of contaminants on pregnancy rate or adult mortality. This spectrum of data-rich to data-poor steps in predicting population consequences of multiple stressors is ubiquitous in conservation and ecological studies2,47. The funding to fill knowledge gaps with empirical data may be lacking, or in the case of critically endangered species, time to wait for science to fill data gaps may be insufficient48. Some authors use expert elicitation49,50 to fill data gaps. Expert opinion or examination of hypothetical, but plausible scenarios should be used to augment rather than replace the available data.

The case study presented here illustrates the use of PVA as a method to inform difficult conservation decisions, by simulating across plausible ranges of uncertainty. For example, sensitivity analyses revealed that some factors (e.g., individual variability in breeding success) have no effect, and such knowledge gaps should not be a barrier to management action. Given our inability to manage some insidious threats, such as persistent organic pollutants that are already in the environment, it is reassuring that the model predicts that this stressor has the smallest adverse impact on the population, at least via the pathway of reduced calf survival. The PVA can focus priority research on questions that make a practical difference. Studies of foraging efficiency under varying levels of anthropogenic disturbance are needed only because the population is prey-limited. If doubling Chinook salmon numbers were possible, and returning them to levels seen in the 1920s51, consideration of other anthropogenic impacts on the whales' foraging efficiency might not be necessary. Alas, this is not a realistic scenario, and the model therefore points to the importance of including both improvement in prey abundance and reduction in noise as the more effective mitigation pathway.

Unfortunately, focus on only the immediate, tractable threats is all too common in conservation. For example, conservation of grizzly bears ( Ursus arctos horribilis) in the continental United States focuses on roads and development activities, but the primary concern is that the species has been absent from most of its range since the 1800s52. Similarly, the current small size of the SRKW population was not caused by lack of salmon. The whales' depleted status is due in large part to the legacy of an unsustainable live-capture fishery for display in aquariums53. Salmon, noise, and contaminants are important factors that can prevent recovery. Many policies, including the US National Environmental Policy Act, require regulators to consider the effect of a proposed activity "which results from the incremental impact of the action when added to other past, present, and reasonably foreseeable future actions regardless of what agency (Federal or non-Federal) or person undertakes such other actions (40 CFR § 1508.7)." Allocating impacts among multiple ocean user sectors may be difficult, but in the case study we present, the population is sufficiently imperilled that it has little or no scope for tolerating additional stressors.

Methods

The SRKW population is closed to immigration and emigration, every individual in the population is known, and the population has been censused annually for decades11. Individuals were identified by their unique fin shapes, saddle patches, and the presence of any nicks or scratches, and sexed using distinctive pigmentation patterns around the genital slits. Male and female offspring remain within the natal, matrilineal unit, although mating occurs within and between these pods. The term "resident" refers to their residency in inshore waters of southern British Columbia (Canada) and Washington state (USA) in the summer months, when they feed almost exclusively on Chinook salmon13,14,54,55. Given that there is no dispersal from the population56, mortality was recorded if an individual's matriline was observed in the population within a year but the individual did not appear.

We used values of demographic parameters calculated from the census data to build the population model in the Vortex PVA program17,18. We included temporal variation in demographic rates ("environmental variation"), based on inter-annual variability in parameters observed since 1976, and we included individual variation in age of maturity and probability of reproductive success. The Vortex simulation model of possible future population trajectories includes demographic stochasticity (binomial variation in individual fates); random assignment of sex and a bi-sexual mating system, resulting in fluctuations in sex ratio and mate availability that can affect small populations; and projections of loss of genetic diversity, allowing for inclusion of inbreeding depression. We quantified population growth as the mean exponential rate of increase (r = ln[N t+1/N t]).

Modelling was conducted in stages. First, a "Baseline" model was developed to represent the population trajectories if demographic rates remain the same as have been observed in recent decades. We confirmed this Baseline model by comparing simulated dynamics with recent population trends. Secondly, we conducted sensitivity tests on uncertain demographic rates in the model to determine which parameters had large effects on the projected population growth. Thirdly, we used a set of models of Individual Threats that tested ranges of values for the primary threats identified in the recovery plans to determine which would have the greatest effects on population projections. Fourthly, we examined Cumulative Threats scenarios to project the fate of the population if further industrial development increases existing threats and adds new ones. A set of Demographic Management scenarios was then examined to determine the population growth that could be achieved by improvements in demographic rates. Finally, we explored Threat Management scenarios to assess the plausibility of reaching sustained annual population growth of 2.3% given various options for increasing salmon abundance, reducing ocean noise levels, or reducing contaminant levels. The following section describes key parameter estimates used in the model. More detailed description of the modelling methods is presented in Supplementary Information. The input files for the Vortex project are available at http://www.vortex10.org/SRKW.zip and from the Dryad Digital Repository at https://doi.org/10.5061/dryad.46vq7.

Baseline PVA

We started the simulations with the ages, sexes, and pod membership of the killer whales living in 2015. We specified the mother of each animal, where known (for 76 of 80 living animals)57. Based on previous genetic data on paternity58, we specified in the simulation that females would not mate with their father, a son, or a maternal half-sibling. What effect lower levels of inbreeding or the inevitable accumulated inbreeding in a closed population will have on any cetacean is unknown. We modelled inbreeding depression as being caused by recessive lethal alleles, with 6.29 "lethal equivalents" (the negative of the slope of log(recruitment) against the inbreeding coefficient), the mean combined effect of inbreeding on fecundity and first-year survival in a survey of impacts on wild species59.

Demographic rates were calculated from individual animal histories compiled by the Center for Whale Research57, using data collected from 1976 through 2014. The time series begins when the population was depleted by live-captures for display in aquariums60. The time series therefore includes periods of moderate population growth (1976 to 1993), subsequent decline, and approximate stability. Demographic rates were estimated for the age-class groupings used in recent models24,61, except that we set an upper limit for female breeding at 45 y rather than 50 y, because no females in the population have been documented to produce calves at older ages. Thus, we calculated survival and (for adult females) fecundity rates for calves (first year), juveniles (defined as from 1 y through 9 y of age), young mature females (10-30 y), older reproductive females (31-45 y), post-reproductive females (46 y and older), young mature males (10-21 y), and older males (22 y and older). Killer whales can survive many years after reproductive senescence, but estimating maximum longevity is difficult in such a long-lived species62. We set an upper limit of age to 90 y in our models, although only about 2% of females would be expected to reach this age, and only about 2% of males (with higher mortality) would be expected to exceed 50 y. Females stop breeding long before the maximum age, so the long-term population growth would not be affected by the upper age limit unless post-reproductive females benefit the pod in ways other than through their own reproduction.

Mortality for each age-sex class was averaged across the 39 years of data to obtain mean annual rates. We did not try to partition observed mortality into presumed causes of death. The use of these historic data for our Baseline model makes the implicit assumption that the frequency of deaths due to the various causes remains the same as has been observed across recent decades. The variation in mortality observed across years has two components: 1) environmental variation (fluctuations in the probability of survival), and 2) demographic stochasticity (binomial variation in individual fates). To determine how much of the observed variation was due to environmental variation, the variance due to demographic stochasticity can be calculated from the expectation for a binomial process, and then subtracted from the total variation across years. Calculated annual mortality rates (and environmental variation) ranged from a low of 0.97% (SD = 0) for young adult females to 17.48% (SD = 17.96) for calves. Although the lack of evidence for annual variation in the mortality adult females beyond that expected from random sampling of a constant probability might seem optimistic, for long-lived species a low level of annual variation in rates would have negligible effect on long-term population trajectories. We confirmed through sensitivity tests (Supplementary Information) that the environmental variation entered into the population model has no effect on our results.

The breeding system is polygamous, with some males able to obtain multiple mates, females mating with different males over their lifetimes, and mating between and within pods. Males become sexually mature (actively breeding, which may occur several years after they are physiologically capable of breeding) from 12 to 18 y of age. Thus, in the model, each male was assigned an age of sexual maturity by randomly selecting a value from 12 to 18. Variance in reproductive success among individual females and males will cause genetic diversity to be depleted faster and inbreeding to accumulate faster than would occur if mating was assumed random. Information is available on male mating success51, and we incorporated variation in male and female reproductive success in the model (Supplementary Information). Our models project an effective population size that is 37% of the total size, close to an estimate obtained from genetic data58.

Breeding rates, expressed as the proportion of the females of an age class that produce a calf each year, were calculated from annual census data. Rates ranged from 0% for post-reproductive females (age >45 y), to 7.88% (SD = 4.15) for older adult females (age 31-45 y), to 12.04% (SD = 3.54) for young adult females (age 10-30 y).

The upper limit on population size was set to 300, so that carrying capacity (K) would not restrict future population growth except under the best conditions tested. In the projections of current or expected conditions, the SRKW populations never reached this limiting size, and rarely exceeded 150 animals in any of the independent iterations of each simulation. Population recovery was assessed by the mean growth rate each year calculated before any carrying capacity truncation. Thus, the growth rate reflects the demographic potential and is not affected by the limit on population size in the model.

The SRKW population was projected for 100 years. For the initial exploration of parameter uncertainty, the simulation was repeated in 10,000 independent iterations to obtain high precision in mean and variance estimations. For comparisons among alternative management scenarios, less iteration is needed to obtain the relative influence of input values, and tests were run with 1,000 iterations. Sensitivity tests were conducted by varying each basic demographic rate (life table values for fecundity and mortality) over a range of ± 10% around the baseline value. For several model variables that describe other aspects of the population dynamics and are also very uncertain, a wider range of values was tested (see Supplementary Information).

Individual Threats

We explored the effects of three threats identified in the recovery strategies. For each of prey abundance, noise disturbance, and PCB contaminants, we scaled impacts such that the estimated current level of the threat resulted in the mean demographic rates reported over recent decades. Effects of prey limitation were modelled using published relationships linking inter-annual variability in Chinook salmon to inter-annual variability in calf and adult mortality63 and fecundity13,61. A prey index was calculated by dividing the total salmon abundance in each year by its average abundance over the 1979-2008 period63. The relationship of mortality to prey abundance was modelled with a multiplier of baseline mortality that is a linear function scaled to 1 when salmon abundance was at the mean observed level over period of observation: MortalityFactor = 3.0412 - 2.0412 * PreyIndex. The relationship of birth rate to prey was modelled with logistic functions, with the intercept scaled to yield the observed birth rates for young females (12.04%) and older females (7.88%) when PreyIndex = 1. For relationships of form BirthRate = exp(A + B*PreyIndex)/[1 + exp(A + B*PreyIndex)], the function parameters were A = −3.0 and B = 1.0 for young females, and A = −3.46 and B = 1.0 for older females. (See Supplementary Information for more details on these relationships.) To explore the impacts of prey abundance across a range of plausible values, we varied the prey index from approximately the lowest level (0.60) reported since 1978 to approximately the highest level (1.30).

Effects of noise on demography were modelled using the approach outlined in previous analyses of loss of acoustic communication space4,64. We used summertime observations to estimate the proportion of time boats were present (during daylight hours) while the whales were foraging and the reduction in foraging expected with that amount of acoustic disturbance. We calibrated the model of noise impacts so that the mean Baseline demographic rates are obtained at the reported level of disturbance. We then simulated the relative change in foraging time and consequently demographic rates across the spectrum from no noise impact at all, to the upper limit expected if boat disturbance increased from current, already high, levels to 100% of time. We do not have data on the amount of acoustic disturbance in the winter feeding areas, but the modelling based on observed summertime disturbance provides a means to project a range of population consequences if changes in disturbance overall mirror those that are possible in the summertime habitat. Land-based observations have shown that SRKWs reduce their time spent feeding in the presence of boats by 25%65. Vessels are present 85% of the daytime, and SRKWs are foraging in the presence of vessels an estimated 78% of that time. Thus, for the 85% current (baseline) exposure to vessels, feeding is expected to be reduced by 16.6% ( = 85% × 78% × 25%) due to disturbance by boats. To translate the reduction in feeding into its demographic consequences, we multiplied the prey index by a factor of (1 − 0.195 * Noise)/(1 - 0.166) to obtain the proportional availability of prey. This proportion is thus 1 in the current, baseline conditions (Noise = 0.85), 0.965 when vessels are always present (Noise = 1.00), and 1.20 assuming no disturbance from vessels. The noise-modified index of prey availability was then used to determine the consequent mortality and fecundity rates. We recognize that anthropogenic noise can also have less direct effects on wildlife, including disruption of social behaviours and even impeding responsiveness to other sensory modalities66.

Our model of accumulation, depuration, and impact on calf survival of PCBs was based on the approach described by Hall et al.67,68 with modifications in rates for SRKW69. Calves obtain their initial load of contaminants from their dams through gestation and lactation, and females producing calves thereby depurate an estimated 77% of their contaminants67. Otherwise, males and non-breeding females accumulate PCBs in the blubber of at a rate that we varied from 0 to 5 ppm/y in our tests. Few data are available on PCBs in the SRKW population with which to calibrate the model of PCB bioaccumulation, and the levels of PCBs reported in SRKW might have been dropping slowly in recent years. Reported levels in adult female SRKW range from 55 ± 19 ppm sampled in 1993-1996, 37 ± 42 ppm sampled in 2004-2007, and 30 ± 31 ppm sampled in 2008-201330. Our population model generates a mean 28, 55, and 81 ppm PCBs in adult females when bioaccumulation rate is 1, 2, and 3 ppm/y, respectively. Effects of maternal PCB load on calf mortality were modelled using a logistic response function (survival = exp(2.65 − 0.02 * PCB)/[1 + exp(2.65 − 0.02 * PCB)]), fitted to the two observed data points for SRKW (survival = 0.8252) and the nearby northern resident killer whales (survival = 0.9218)24, with the mean PCB levels (55.4 ppm and 9.3 ppm, respectively)70 reported from the time period in the middle of the span over which mortality rates were calculated. If we use the more recent, lower estimates of PCB loads in SRKW to estimate the impacts, our response function would have a steeper slope. There are not yet sufficient data on effects of PCBs on other demographic rates to allow inclusion of any other effects of PCBs (or other contaminants) in our PVA model.

Cumulative Threats

We modelled two scenarios to represent the cumulative impacts of possible increases in threats, based in part on a recent environmental impact assessment submitted to Canada National Energy Board45 evaluating effects of a proposed oil pipeline and associated tanker traffic. For the purposes of this PVA, projected increases in anthropogenic threats are not meant to mimic any one industrial development, but rather a general process of industrialization reflecting the number of port expansions, pipeline proposals, and liquefied natural gas terminal proposals pending for the BC coast4. For a low level scenario, we used the catastrophe option in Vortex to add the possibility of large (>16,500 m ³) and smaller (>8,250 m ³) oil spills. The frequencies of a big spill (0.21% chance per year) and a smaller spill (1.08%) were based on an industry projection of the likelihood of such spills caused by proposed increase in tanker traffic71. Based on the percent overlap of oil coverage and critical habitat, we estimate that if a large oil spill were to occur, about 50% of the SRKWs would be killed due to direct exposure to the oil. We estimate that 12.5% of the SRKWs would be killed by exposure to oil from a smaller spill. For a scenario with higher level impacts of development, we doubled the frequency of oil spills.

These energy development scenarios also included an increase in vessel noise and disturbance of feeding, with the current vessel presence of 85% of time increased to 92.5% in the low level scenario and to 100% in the high level scenario. We also included a probability of additional deaths of killer whales due to ship strikes, with one death per decade in the low level and two deaths per decade in the high level scenario. Although some persistent organic pollutants might increase under increased industrial activity in the SRKW habitat, PCBs have been phased out of production and are in decline in at least some fish species in low-development basins72. Lacking data on likely long-term trends in the contaminant loads of SRKW prey, we did not include any change in such pollutants in these scenarios.

Climate change is projected to cause a decline in Chinook abundance28, and we modelled this possibility with a projected 25% (low scenario) or 50% (high scenario) decrease in Chinook over the next 100 years.

Demographic Management and Threat Management scenarios

We used the PVA to simulate how much improvement in demographic parameters or how much reduction in anthropogenic threats, singly or in combination, would be required to reach a stated recovery objective of sustained annual population growth of 2.3% for 28 years11. In calculating the growth for these models, we started the tally 20 years into the simulation to avoid short-term demographic fluctuations as the age structure adjusts to new demographic rates, and growth was tallied over the subsequent 28 years. For the set of Demographic Management scenarios, we assessed the relationship between improved demography and population growth. Birth rate was incremented by 1.1x, 1.2x, 1.3x, 1.4x, and 1.5x, whereas calf mortality and adult mortality were decreased by 0.9x, 0.8x, 0.7x, 0.6x, and 0.5x. Next, in Threat Management scenarios, we modelled the effects of reduced threats, with the consequences resulting from the functional relationships to demography. We increased salmon abundance (up to the highest level of the Chinook index observed between 1979 and 2008, namely 1.3 times the long-term average). We simulated the improved demography if acoustic disturbance were reduced or eliminated. We considered the population consequences of improved calf survival resulting from reduction of PCBs, testing rates of future accumulation in SRKW from the estimated current 2 ppm/y to down to 0 ppm/y. Finally, we tested scenarios that both reduced acoustic disturbance by half and increased salmon abundance up to 1.3x.

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Acknowledgements

We thank the team members for the Center for Whale Research for providing the complete databases of censuses and demographic trends from 1976 through 2014. We thank Ailsa Hall, Sea Mammal Research Unit, University of St. Andrews, for providing the model of bioaccumulation of PCBs in cetaceans.

Author information

Affiliations

1. Chicago Zoological Society, Brookfield, IL 60513, USA

2. Oceans Initiative, Seattle, WA 98102, USA

3. Center for Whale Research, Friday Harbor, WA, 98250, USA

Kenneth C. Balcomb III

& Deborah A. Giles

4. College of Life & Environmental Sciences, University of Exeter, Exeter, Devon, EX4 4QG, UK

Lauren J. N. Brent

& Darren P. Croft

5. Cornell Lab of Ornithology, Cornell University, Ithaca, NY, 14850, USA

6. Raincoast Conservation Foundation, Sidney, BC V8L 3Y3, Canada

Misty MacDuffee

& Paul C. Paquet

7. University of Victoria, Victoria, BC V8P 5C2, Canada

Contributions

P.P. coordinated the project. K.C.B. and D.A.G. provide the core census and demographic database. R.W., E.A., L.J.N.B., C.W.C., D.P.C., P.P., and M.M. provided data on threats. R.C.L. built the population model and conducted the simulations. R.W., R.C.L. and P.P. led the writing. All authors contributed to and reviewed the manuscript.

Corresponding author

Correspondence to Robert C. Lacy.

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Adrian M. Tuohy

, John R. Skalski

& Nick J. Gayeski

Fisheries (2019)

# data[].attributes.attachment_link.title
Evaluating anthropogenic threats to endangered killer whales to inform effective recovery plans

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Understanding cumulative effects of multiple threats is key to guiding effective management to conserve endangered species. The critically endangered, Southern Resident killer whale population of the northeastern Pacific Ocean provides a data-rich case to explore anthropogenic threats on population viability.

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PCBs, or polychlorinated biphenyls, are industrial products or chemicals.

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The effects PCBs have on large animals may not be as obvious, but we are finding that they accumulate in the blubber, killing orcas and decreasing the ability of the populations to recover.

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Introduction

The severe impact on top predators of the bioaccumulation of DDT and other organochlorine (OC) pesticides in food webs was first identified in the early 1960s1. Most OC pollutants were banned in developed countries in 1970s-1980s and some terrestrial wildlife populations recovered. Experimental studies have established that OC pesticides and the more persistent polychlorinated biphenyls (PCBs) have a range of species-specific and dose-dependent toxic effects such as immunosuppression and reproductive impairment in all mammalian species tested, including marine mammals4,5,6,7. However, the impact of historic and current exposure to marine pollutants on European cetacean top predators is still largely unknown.

To investigate this issue we conducted a meta-analysis of European data on summed 18-25 chlorobiphenyl congeners (∑PCB) concentrations (mg/kg lipid weight (lw)) in cetaceans that were stranded and necropsied or free-living and biopsied. Data came from 1,081 animals of four species:- harbour porpoise ( Phocoena phocoena, HP)(n = 706), striped dolphin ( Stenella coeruleoalba, SD)(n = 220), bottlenose dolphin ( Tursiops truncatus, BND) (n = 131) and killer whale ( Orcinus orca, KW)(n = 24). The ∑PCB was mainly derived from two different laboratories, but with both using internationally standardised methodology enabling full integration of data. The analysis included statistical evaluation of long-term temporal trends in ∑PCB concentrations in UK-stranded HPs (1990-2012) and Mediterranean SDs (1990-2009). We compared mean ∑PCB concentrations in all four species with a range of established PCB toxicity thresholds for marine mammals. The lowest PCB toxicity threshold was a widely used and relatively low PCB toxicity threshold for onset of physiological impacts and equivalent to 9 mg/kg lipid as ∑PCB6 in this study. We also used the very highest PCB toxicity threshold reported for marine mammals, for profound reproductive impairment in ringed seals ( Phoca hispida) in the Baltic Sea and equivalent to 41mg/kg lipid as ∑PCB in this study6.

We compared mean PCBs concentrations in UK-stranded HPs that were "healthy" and died of acute physical trauma (n = 345) (control group) with mean PCBs concentrations in HPs that died of infectious diseases (n = 252) (case group) or starvation (n = 42). Where data permitted, sex differences in mean PCB concentrations were investigated to assess maternal offloading of PCBs via lactation. Finally, we reviewed the current population and reproductive status of the extant odontocete populations in European waters using systematic local and international observational survey and other data collected over the past 15-20 years (e.g. International Union for Conservation of Nature assessments)8.

Results

Spatial and temporal trends and sex differences in ∑PCB exposure

The temporal trend in ln ∑PCB lipid concentrations in UK HPs (1990-2012) and SDs from the western Mediterranean Sea (1990-2009) is shown in Fig. 1A,B. The temporal trend in both populations was highly statistically significant (p < 0.001). In UK-stranded HPs, ln ∑PCB concentrations declined slowly from 1990 to 1998 and then remained relatively stable from 1998 to 2012 against the null hypothesis of no trend (p < 0.001, F = 11.76, residual df = 701.97, trend df = 3.03) ( Fig. 1A). In Mediterranean SDs, ln ∑PCB concentrations showed a marked decline from an initial peak in 1990, but then stabilized from 2003 to 2008, but with blubber ∑PCB concentrations still consistently exceeding all mammalian toxicity thresholds. The trend is statistically significant (p < 0.001, F = 55.45, residual df = 212.03, trend df = 6.97) against the null hypothesis of no trend ( Fig. 1B).

Temporal trends in ∑PCBs in UK-stranded harbour porpoise ( Phocoena phocoena) and striped dolphins ( Stenella coeruleoalba) in the western Mediterranean Sea.

To assess the ∑PCBs trend we have fitted a Generalised Additive Model (GAM) to the data using the R (R Development Core Team, 2013) package mgcv. We used thin plate regression splines to do the smoothing and the degree of smoothing was determined by generalised cross validation. (A) Ln ∑PCBs (sum 18-25CB) mg/kg lipid concentrations in UK harbour porpoise blubber against date for all data for 1990-2012 (n = 706). The continuous line represents the smoothed trend from a Generalized Additive Model fitted to the data. The trend is statistically significant (p < 0.001, F = 11.76, residual df = 701.97, trend df = 3.03) against the null hypothesis of no trend. The dashed lines represent the 95% bootstrapped Confidence Intervals. The yellow line represents ln ∑PCBs equivalent to 20.0 mg/kg lipid and the red line 40 mg/kg lipid. (B) Ln ∑PCBs (sum 18-25CB) lipid concentrations in biopsied striped dolphin blubber from the Mediterranean Sea against date for all data for 1990-2009 (n = 220). Figure shows the natural logs (ln) of the whole data set plotted against the date found. The continuous line represents the smoothed trend from a Generalized Additive Model fitted to the data. The trend is statistically significant (p < 0.001, F = 55.45, residual df = 212.03, trend df = 6.97) against the null hypothesis of no trend. The dashed lines represent the 95% bootstrapped Confidence Intervals. The yellow line represents ln ∑PCBs equivalent to 20.0 mg/kg lipid and the red line 40 mg/kg lipid.

Some geographical regions in this study were global PCB "hotspots" for cetaceans. Mean ∑PCB lipid concentrations in BNDs and KWs from the NE Atlantic and in BNDs and SDs from the Mediterranean were among the highest recorded in cetaceans globally9, with males and females markedly exceeding all known PCB toxicity thresholds for marine mammals ( Figs 2, 3, 4, 5). Results of kernel smoothing estimates show very high risk of PCB toxicity for KWs in NE Atlantic, BNDs off SW Iberia and in the northern Adriatic Sea and BNDs/SDs in the western Mediterranean ( Fig. 6). ∑PCB data from biopsies of 152 free-living individuals constituted 38/131 (29.0%) of all BNDs; 99/220 (45.0%) of the SDs; and 15/24 (62.5%) of the KWs in this study. All HPs in the UK were stranded. Although biases can potentially occur with opportunistically sampled stranded cetaceans, the study population used here consisted of both compromised diseased individuals as well as healthy trauma cases and no clear differences between mean ∑PCB concentrations in stranded and biopsied BNDs (1990-2012), SDs (1991-2009) and KWs (1994-2012) were observed ( Fig. 7). More specifically, mean ∑PCB concentrations in stranded male and female SDs were slightly higher than biopsied male and female SDs but biopsied male BNDs had slightly higher ∑PCB concentrations than stranded male BNDs. For KWs, biopsied males and stranded females had higher ∑PCB concentrations than stranded male and biopsied female KWs, respectively ( Fig. 7). Box and whisker plots (male v female) were generated for ∑PCB and ln ∑PCB concentrations in all stranded and biopsied HPs (1990-2012), BNDs (1990-2012), SDs (1990-2008) and KWs (1994-2012) ( Fig. 8A-D).

( A-D) Distribution map (smooth mean density kernel plots) of ∑PCBs data points in Europe - all cetacean species (all ages) from 1996-2012. (A) - HPs (n = 548); (B) - BNDs (n = 110); (C) - SDs (n = 71) and (D) - KWs (n = 21). Spatial distribution of ∑PCB lipid concentrations produced in Esri ArcMap 10.1 (www.esri.com). Maps are displayed in the WGS84 co-ordinate system. Data points are shown along with local averages. These averages were calculated by kernel smoothing using a polynomial order 5 kernel with power = 0, ridge parameter = 50 and bandwidth based on the spatial distribution of the observations for each species: bottlenose dolphin 0.75 degrees; harbour porpoise 0.5 degrees; killer whale 1.2 degrees; striped dolphin 0.5 degrees. Both the data points and the local averages are displayed in three colours: yellow (∑PCB concentration =  < 20 mg/kg); orange (∑PCB concentration = 20-40 mg/kg lw); and red (∑PCB concentration =  > 40 mg/kg lw).

( A-D) Box and whisker plots for male (M) v female (F) v unknown sex (U) were generated for ∑PCB and ln ∑PCB concentrations for ( A) all stranded HPs (1990-2012); ( B) stranded or biopsied SDs (1990-2008); ( C) stranded or biopsied BNDs (1990-2012); and ( D) stranded or biopsied KWs (1994-2012). The lower line (blue) is the lower PCB toxicity threshold (=9.0 mg/kg lipid, as ∑PCB) for onset of physiological effects in experimental marine mammal studies6. The upper line is the highest PCB toxicity threshold (=41.0 mg/kg lipid, as ∑PCB) published for marine mammals based on marked reproductive impairment in ringed seals in the Baltic Sea6.

We compared ∑PCB concentrations among regions within the NE Atlantic and Mediterranean Sea. Since our ∑PCB data is lognormal, we are able to use the sample geometric mean to estimate the population median ( Tables 1 and 2) and that this estimator is unbiased for doing this10. Mean ∑PCB concentrations and geometric means (with upper and lower 95% confidence intervals) were generated for males and females of each cetacean species and region for all available data (n = 1,009) ( Table 1) and for adults only (n = 401) ( Table 2). These tabulated data were presented along with minimum and maximum values (i.e. range) for males and females for each species and region ( Tables 1 and 2). In general, the ∑PCB sample geometric means (as estimator of population median values) were 25-65% lower than the (arithmetic) means for the same species, but still exceeded even the very highest marine mammal PCB toxicity threshold (∑PCB = 41 mg/kg lipid) for some BND, SD and KW groups in both NE Atlantic and Mediterranean Sea regions ( Tables 1 and 2).

Table 1 ∑PCBs exposure (mean; sample median; geometric mean with upper and lower 95% CI; range) (mg/kg lipid) by species, region and sex (all ages).

Table 2 ∑PCB exposure (mean; sample median; geometric mean with upper and lower 95% CI range) (mg/kg lipid) by species and region (sexually matures only).

For males and females (all ages), high mean ∑PCB concentrations (>100.0g/kg lw) were found for BNDs off Iberian Peninsula (NE Atlantic), western Mediterranean and northern Adriatic Sea; for SDs in western Mediterranean and for KWs (NE Atlantic) ( Fig. 2). Among adults, high individual female ∑PCB concentrations (>100mg/kg lw) were found in KWs from all NE Atlantic regions, in BNDs from England and Wales and in SDs from the western Mediterranean Sea ( Table 2). Mean ∑PCB concentrations in adult female KWs (176.8 mg/kg lipid) in the NE Atlantic greatly exceeded mean concentrations in adult female southern resident (55.4 mg/kg lipid) and transient (58.8 mg/kg lipid) KWs10 off British Columbia (NE Pacific). Adult female KWs in the UK and Ireland had the highest mean ∑PCB concentrations (224.8 mg/kg lipid) followed by KWs in the Strait of Gibraltar (215.4 mg/kg lipid). Mean ∑PCB concentrations in adult female BNDs (61.8-158.3 mg/kg lipid) and SDs (84.5-523.7 mg/kg lipid) in some western European populations also markedly exceeded those in southern resident and transient KWs off British Columbia10 ( Fig. 3)( Table 2). Mean ∑PCB concentrations greatly exceeded all marine mammal PCB toxicity thresholds in mature ( Fig. 3) and immature ( Fig. 4) BNDs, SDs and KWs. Individuals for which the maturity status could not be established, mean ∑PCB concentrations still exceeded all marine mammal toxicity thresholds in BNDs and SDs ( Fig. 5).

The toxicological data show that these populations greatly exceed concentrations at which severe toxic effects are known to occur. Pathological findings on necropsy consistent with immunosuppression and increased susceptibility to disease included macro-parasitic and bacterial pneumonias, high lung and gastric macro-parasite burdens and generalised bacterial infections (septicaemias). These were regularly found on necropsy in stranded HPs5, BNDs and KWs. In Mediterranean SDs distemper due to cetacean morbillivirus (CeMV) infection9 was frequently seen. Several stranded KWs also had multiple dental infections leading to large mandibular abscesses identified on necropsy12. High ∑PCB contamination can cause immunosuppression7 and may be a significant contributing factor in the death of many of the stranded individuals that had fatal infectious diseases on necropsy.

For necropsied cetaceans stranded in the UK (1990-2012), ∑PCB data was obtained for 706 HPs, 38 BNDs and 7 KWs ( Tables 1 and 2). For BNDs (UK), causes of death included trauma (n = 5 male; n = 2 female); infectious disease (n = 2 male; n = 4 female). For the UK-stranded KWs, causes of death included starvation (n = 2), infectious disease (n = 2) and live stranding (n = 2). A cause of death could not be determined for 25 HPs, 11 BNDs and 1 KWs. ∑PCB lipid concentration in UK-stranded male HPs of all ages from 1990-2012 was significantly higher (sample mean = 19.4 mg/kg lw; sample median = 11.5 mg/kg lw; n = 388) than for females of all ages (sample mean = 13.8 mg/kg lw; sample median 8.35 mg/kg lw; n = 318) (ANOVA, P < 0.001) ( Fig. 2).

∑PCB lipid concentrations in subgroups of "healthy" male UK-stranded HPs that were generally in good nutritive condition and died of acute physical trauma (sample mean = 13.8 mg/kg lw; sample median = 9.57 lw; n = 201) had significantly lower ∑PCB than male HPs that were in poorer condition and died of a range of infectious diseases (sample mean = 26.5 mg/kg lw; sample median = 18.9 mg/kg lw; n = 120) (ANOVA, P < 0.001). In female UK-stranded HPs that died of acute physical trauma, ∑PCB lipid concentrations (sample mean = 8.50 mg/kg lw; sample median = 6.41 mg/kg lw; n = 144) were significantly lower than female HPs that died due to a range of infectious diseases (sample mean = 16.8 mg/kg lw; sample median = 12.2 mg/kg lw; n = 132) from the same period (ANOVA, P < 0.001) ( Fig. 2). Male and female HPs that died of starvation were all in a poor or emaciated condition. Both male HP starvation cases (sample mean = 20.7 mg/kg lw; sample median = 12.5 mg/kg lw; n = 26) and female HP starvation cases (sample mean = 27.9 mg/kg lipid; sample median = 9.74 mg/kg lw; n = 16) had higher ∑PCB concentrations than the physical trauma group. For UK-stranded HPs (both sexes), mean ∑PCB mg/kg lipid was 150-328% greater in infectious disease or starvation cases as compared to trauma cases. The increase in ∑PCB on a sample median basis was 130-198% greater for HP disease or starvation cases as compared to HP trauma cases.

Population Dynamics

Such sustained and elevated PCB burdens are likely to have significant effects at the population level in European BNDs, SDs and KWs. Although we cannot directly and causally link high ∑PCB exposures to cetacean population declines, many of these populations are either very small, or show evidence of major and long-term declines or a significant contraction of range. Only very small KW populations are now found in industrialised regions of Europe. There is only one resident population in southern Europe14: a tuna-feeding KW subpopulation in the strait of Gibraltar comprising two pods totalling 36 individuals13. These animals have been monitored every year since 1999. Only six mature females were reported to have calved between 1999 and 2011 and these produced only five calves living more than 1 year. This 6.4% annual female fecundity rate over a 13-year period is one of the lowest recorded reproductive rates for KWs globally and the subpopulation was recommended for listing as "Critically Endangered" due to small population size14. Around NW Scotland and Western Ireland, a small group of only nine KWs is regularly seen15. This group of marine-mammal-eating KWs comprises four adult males, two adult females and three adult female or sub-adult males. Although studied over a 19-year period, no calves have ever been reported within this group15. No other resident or coastal KW groups are found off the Iberian Peninsula or in the Bay of Biscay, although occasional offshore KW sightings occur (e.g.16). Long-term cetacean stranding records in the Netherlands show that KWs were first recorded on the Dutch North Sea coastline in 1783, observed regularly from 1918 to 1963 and completely ceased thereafter until two single KW strandings in 2009 and 201017.

Historic strandings data suggest that multiple BND resident or coastal groups in Europe became depleted or locally extinct in the late-1960s to mid-1970s, including those in the UK (e.g. Morecambe Bay; East coast of England)18 and the North Sea Dutch coast19. The last member of a resident BND population at Arcachon, France, died in 200320 and the small resident BND group (current census n = 27) in the Sado Estuary, Portugal, showed decline due to low calf survival over several decades21. Blubber PCB levels for two females and one male BND (sampled between 1995 and 1997) from this population ranged from 37.1 to 114.0 mg/kg lw. The Mediterranean Sea remains a global PCB hotspot1 where most of the extant marine mammal species, including SDs, BNDs and short-beaked common dolphins (CDs)( Delphinus delphis) have declined over decades14,22. The current IUCN Red List conservation status of BNDs and SDs in the Mediterranean Sea is "Vulnerable". The Mediterranean CD subpopulation is now classified as "Endangered" after experiencing major and generalized decline over the last 40-50 years, particularly in the northern Adriatic Sea and in the eastern Ionian Sea8. Blubber PCB concentrations are significantly higher in CDs and SDs in the Mediterranean Sea compared to the much more abundant NE Atlantic populations23.

For HPs in the NE Atlantic, a single continuous population ranges from France to northern Norway. A separate much smaller Iberian population is estimated to comprise only 4,398 (CV = 0.92) porpoises24. In the Baltic Sea, two separate HP subpopulations exist: one in the western waters (Kattegat, the Belt Seas) estimated at 40,475 individuals (CV = 0.235) and listed as "Vulnerable" (by HELCOM)25 and another in the Baltic Sea proper, which is now very small and has suffered decades of decline and is listed as "Critically Endangered"8. A history of hunting, high chemical pollutant exposure and accidental entrapment in commercial fishing gear (bycatch) are thought to have been responsible for this decline24. A total of 375,358 (95% CI = 256,304-549,713) porpoises was estimated for EU Atlantic continental shelf waters including the Iberian and western Baltic (sub-)populations (July 2005)16. For the NE Atlantic (UK) HP population, a longer calving interval, lower pregnancy rate and later maturation and higher rates of reproductive abnormalities were also recently identified in a necropsy study of 329 female UK-stranded HPs (1990-2012), as compared to HP populations in much less PCB-polluted regions like Iceland and the Gulf of Maine/Bay of Fundy (NW Atlantic)26. Direct observations of reproductive failure (foetal death, abortion, dystocia or stillbirth) were observed in 25/127 (19.7%) of necropsied mature female HPs in the same study26.

Consideration of alternative causes of mortality

Accidental entrapment in commercial fishing gear (bycatch) is often considered to be the greatest conservation threat globally to small cetaceans8,27. In UK strandings and necropsy data (1990-2013 inclusive) bycatch was diagnosed as the cause of death for 296/615 (48.1%) of UK-stranded common dolphins ( Delphinus delphis) (CDs) and 338/1983 (17.0%) of HPs. In contrast, only 9/130 (6.9%) UK-stranded SDs; 4/71 (5.6%) BNDs and 0/7 (0.0%) KWs were diagnosed as bycatch during the same period. Bycatches recorded under the 2013 UK dedicated bycatch sampling programme included 101 days on pelagic trawls and 346 days on static gear vessels and included observed bycatches of 18 HPs, 11 CDs, two SDs and a single BND. Six common dolphins were recorded in pelagic trawls. All other cetacean bycatches were recorded from static net fisheries. Preliminary bycatch estimates for the entire UK fleet during 2013 from systematic observer-based studies provided estimates of HP bycatch of around 1917 animals assuming no pingers (acoustic bycatch deterrent devices) were used (CV = 0.126) and 1652 animals if all UK boats over 12 m used pingers correctly (under EU regulation 812)(CV = 0.147)28. Other estimates for the entire UK fleet in 2013 indicate around 320 CDs and around 470 seals were bycaught28. Bycatch of BNDs, however, was considered too rare to estimate for the entire UK fleet and KW bycatch was not recorded28. A bycatch observer study for the Irish albacore tuna ( Thunnus alalunga) drift-net fishery undertaken in offshore waters of the NE Atlantic in the 1990s found the highest bycatch rates in CDs followed by SDs, with much lower numbers of bycaught BNDs and no KW bycatch29. The highest bycatch rates generally occur in the most numerically abundant species in the NE Atlantic region, HPs and CDs, but with much lower rates of bycatch in BNDs and bycatch unrecorded in KWs in recent years30. Very low numbers of bycatches were found in the long-term observer-based studies of the resident European BND populations:- BNDs in Shannon estuary, Ireland (population size = 107-140; zero bycatch recorded since 1993)[S. Berrow, unpublished data]; Sado estuary, Portugal (population size = 27; zero bycatch recorded from 1983-2013) (Manuel E. Dos Santos, pers. com.) and Slovenia, northern Adriatic Sea (population size estimate = 74; 95% CI = 57-90; 2 cases of bycatch since 2002) [T. Genov, unpublished data, see also31]. Collectively, these necropsy and fisheries bycatch observer studies from approximately 1990 onwards indicate that bycatch is unlikely to be driving population declines of BNDs or KWs around the UK or in the wider NE Atlantic during this period.

Other potential causes of cetacean mortality include ship-strike; acoustic disturbance from high-intensity/anthropogenic acoustic sources; nutritional limitation caused by reduced prey availability (e.g. overfishing or climate change); biotoxins (harmful algal blooms) and infectious disease (e.g. cetacean morbillivirus, CeMV)32. Using CSIP UK strandings and necropsy data (1990-2013 inclusive) ship-strike was a relatively infrequent cause of death accounting for only 17/1983 (0.8%) stranded HPs; 0/130 (0.0%) SDs; 0/71 (0.0%) BNDs and 0/7 (0.0%) KWs necropsied in the UK. All tests for biotoxins in UK-stranded cetacean tissues were negative (or at trace levels) since 199032,33.

The potential impacts of anthropogenic high-intensity acoustic sources on cetaceans include mass stranding events (MSEs) that have occurred on a global basis, predominantly involving beaked whales exposed to mid-frequency active sonars in naval exercises. Non-beaked whale MSEs with a probable acoustic cause have occurred, such as a 2008 CD MSE in the UK, but are very rare in European waters32. No acoustically-induced MSEs were recorded in HPs, SDs, BNDs or KWs in European waters. Acoustically-induced cetacean MSEs have been recorded in the Mediterranean Sea but also primarily involved beaked whales36,37.

In the Mediterranean and Black Seas, all cetacean species where population assessments have occurred are considered to be declining. A range of threats has been proposed including hunting (historically); bycatch; overfishing/prey depletion; habitat degradation; morbillivirus infection and chemical and acoustic pollution. Empirical evidence for the effects of prey depletion (e.g. due to overfishing or climate change effects) leading to nutritional limitation is limited for cetaceans, but diet/nutrition effects have been linked to recruitment in KWs and fin whales ( Balaenoptera physalus) [reviewed in26]. Such processes would potentially increase PCB toxicity in malnourished animals by mobilising lipophilic PCBs from blubber to other body compartments7,23. A recent global review of Cetacean Morbillivirus (CeMV) found that SDs have been negatively impacted by CeMV epizootics in 1990-1992 and 2006-200838 and probably again in 2011 in the western Mediterranean39. The largest CeMV epizootic in 1990-1992 was associated with very high PCB concentrations9. A CeMV epizootic also occurred in long-finned pilot whales ( Globicephala melas) in the Mediterranean Sea in 2006-200740. In contrast, only small periodic CeMV-related mortalities have occurred in individual cetaceans in NE Atlantic region38. No large scale epizootics of CeMV38 or of any other pathogens are known to have occurred in any cetacean species in NE Atlantic region since 1990.

Discussion

The stabilised temporal trends in blubber PCB concentrations in cetaceans in Europe contrast with other industrialised northern hemisphere regions, such as North America, where PCBs have continued to decline in BND41 and KW11,23 populations. PCBs were banned in closed systems in the USA in 19791 and in 1981 in the UK4, but were not phased out until 1987 in European countries that border the Mediterranean Sea1,42. Mean ∑PCB concentrations in adult female KWs in our study substantially exceeded concentrations in both southern resident and transient female KWs off British Columbia11,23. Where females are reproducing normally, blubber PCB concentrations are known to fall significantly with successive pregnancies due to maternal offloading through gestation and lactation. The relatively high ∑PCB concentrations in many adult female KWs in this study is consistent with reproductive failure in at least some individuals, due to either adult females failing to offload PCBs to calves during pregnancy and lactation7 or re-accumulation of dietary PCBs in some post-parturient and reproductively senescent KWs11.

Mean blubber ∑PCB concentrations in male KWs in this study were higher than male "southern resident" KWs off British Columbia (NE Pacific) in the 1990s and were only slightly lower than male "transient" (marine mammal eating) KWs from the same region11,41. Very high mean PCB concentrations have been recorded in blubber biopsies of adult male (n = 4) marine mammal-eating West Coast "transient" KW ecotype off California, USA (mean ∑PCB = 630 mg/kg lipid)43; in individual stranded KWs in Oregon State23; and in a transient adult female that stranded in Washington State in 2002 with ∑PCB = 1,100 mg/kg lipid44. For BNDs, only a population in a highly polluted Superfund site in Brunswick, Georgia (USA) exposed to a major point source of PCB pollution with Aroclor 1268 45 had mean exposures similar to many BND groups in our study. HP blubber ∑PCB concentrations in this study were similar to those associated with immunosuppression and infectious disease mortality in previous multivariate studies of UK-stranded HPs (statistically independent of age, sex, sexual maturity and two quantitative indices of nutritional status)5 and similar to those associated with impaired reproduction in adult female HPs in UK waters26.

A large number of factors can influence PCB exposure and subsequent PCB concentrations in blubber including, but not limited to, blubber sample condition, diet, degree of maternal offloading, year of sampling, season, age, gender, location, species, body condition and whether or not an animal was sampled in good health. Some of these we can control for statistically as potentially confounding factors, others we cannot. Nevertheless, for SDs, BNDs and KWs around the Iberian Peninsula (both NE Atlantic and Mediterranean regions), mean and median ∑PCB concentrations levels were among the highest recorded for cetaceans globally, regardless of sample type/nutritional condition/sex/year of sampling, etc. In terms of blubber sample quality, we are able to obtain 954/1081 ( =  88.3%) fresh or slightly decomposed stranded or biopsied blubber samples, effectively negating the potential bias of sample degradation on PCB determination. Nor did we see any significant overall differences in mean ∑PCB concentrations between stranded and biopsied BNDs, SDs or KWs. This shows that the ∑PCB concentrations in stranded animals were not fundamentally biased in comparison to the free-living biopsied cetaceans.

In relationship to nutritional status, we can show that both male and female HPs that died of trauma had the lowest ∑PCB concentrations and this increased by 190-198% for infectious disease cases and by 130-328% for starvation cases. Although we lack data to test this "nutritional loss" effect rigorously on ∑PCB concentrations in SDs, BNDs and KWs, we can show that the excessively high ∑PCB concentrations occurred in virtually all individual SDs and BNDs around the Iberian Peninsula and for virtually all individual KWs across the NE Atlantic region, irrespective of blubber sample quality, year of sampling, season, gender, nutritive condition and whether or not an animal was sampled in good health.

There are also marked species-specific variations in susceptibility to PCB exposure. The lower PCB toxicity threshold used in this study was predominantly derived from non-cetacean species such as seals, otters and mink7. It is well recognized that mink are one of the most PCB-sensitive species and so it is highly possible that cetaceans are less sensitive to PCB exposure than species like mink. If so, the use of the Kannan threshold7 is likely to overestimate the true PCB risk to cetaceans. However, this lower PCB toxicity threshold is equivalent to only 9 mg/kg lipid (as ∑PCB) - whereas many BND, SD and KW groups in this study had one order of magnitude greater mean or median ∑PCB concentrations (50-350 mg/kg lipid). So, even if the lower PCB toxicity threshold does significantly over-estimate the likely toxicity of PCBs on cetaceans - the very high ∑PCB exposures recorded empirically in European cetaceans in this study (>1,000% greater than 9 mg/kg lipid) still provides compelling evidence for the inherent PCB toxicity risk in this study.

Current threats to cetaceans from persistent organic pollutants (POPs) in Europe appear to be restricted to PCBs. Marked and ongoing declines in tissue concentrations of organochlorine pesticides (e.g. DDTs) have occurred in UK-stranded HPs4 and in western Mediterranean SDs3 and BNDs42. Similar marked declines in tissue contaminants have occurred in UK HPs for butyltins46 and brominated flame retardants following a 2004 EU-ban4. Other newer chemical compounds including the alternative brominated and chlorinated flame retardants such as tetrabromo-p-xylene (TBX), tetrabromo-o-chlorotoluene (TBCT) and 2,3-dibromopropyl-2,4,6-tribromophenyl ether (TBP-DBPE) and Dechlorane Plus (DDC-CO) isomers47, perfluoroalkyl substances (PFASs) such as perfluorooctane sulphonate (PFOS) and perfluorooctanoic acid (PFOA) in48 and emerging organophosphorus flame retardants (PFRs) and plasticisers49 were detected in some UK-stranded HP samples and with the possible exception of PFOS, were at either very low levels or occurred below levels of analytical detectability.

Many European seas (e.g. Baltic, Mediterranean and North Seas) are surrounded by highly industrialised land masses with high human population densities which may at least partly explain the high PCB exposures we have detected1. Mass production of PCBs commenced in 1929, reaching peak levels in the 1960s and 1970s, when many European cetacean populations already appear to be declining. Nearly 97% of the historical use of PCBs occurred in the northern hemisphere50, with the marine environment acting as the ultimate PCB "sink". By the late 1990s, however, only 1% of globally manufactured PCBs were estimated to be in sea water, with 6-7% in marine sediments (reviewed in1), while as of 2005, 1.1 million tons of PCB contaminated material still required disposal by EU Member States, most notably France and Spain51. PCB effects are likely to be particularly pernicious in highly exposed European BND, SD and KW populations by markedly suppressing reproduction and probably subsequent recruitment at individual and population levels. EU regulations to mitigate PCB pollution currently appear insufficient to protect cetacean top predators in the NE Atlantic and Mediterranean Sea. As sentinels of marine ecosystems, monitoring PCB concentrations in marine mammals should be considered for inclusion as an indicator under descriptor 8 within the European Marine Strategy Framework Directive (MSFD) (Directive 2008/56/EC). Our results indicate that European marine mammal habitats are unlikely to meet Good Environmental Status within the MSFD by 2020 and that several dolphin species are unlikely to achieve Favourable Conservation Status now under EC Habitats Directive (Council Directive 92/43/EEC). Further steps to reduce PCB inputs into the European marine environment should include stricter controls on disposal of PCBs, e.g. in buildings with sealants containing PCBs4,52. Also, measures should be taken to limit PCB bioavailability to marine food webs, such as improved management of dredging of harbours/ports, as well as improved containment of PCB environmental contamination from industrial buildings/equipment and domestic waste disposal (e.g. landfill).

In conclusion, this pan-European meta-analysis of stranded or biopsied cetaceans demonstrates that several European cetacean species, specifically BNDs, SDs and KWs, currently have markedly elevated blubber PCB concentrations. Particular "PCB hotspots" included the western (SDs and BNDs) and central (BNDs) Mediterranean Sea and SW Iberia, the Gulf of Cadiz (BNDs) and the Strait of Gibraltar (BNDs and KWs). Despite an EU ban on the use and manufacture of PCBs in the mid-1980s, blubber PCB concentrations are still very high, possibly having reached a "steady state" between environmental input and degradation, meaning that high PCB exposures are set to continue for the long-term in cetacean top predators in Europe. These high and stable PCB exposures are associated with small populations, long-term population declines or contraction of range in several dolphin species in Europe (NE Atlantic and Mediterranean Seas) that were not adequately explained by other factors (e.g. bycatch or other anthropogenic causes of mortality). Bycatch is common in the most abundant cetacean species in Europe, but is comparatively rare in BNDs and virtually unrecorded in recent years for KWs, suggesting that the ongoing population declines in these two species are predominantly driven by other processes, with bioaccumulation of PCBs through marine food chains being the predominant factor. A lack of recruitment in monitored KW and BND populations is also consistent with PCB toxicity as the likeliest cause of their declines. In the Mediterranean Sea, the SD has suffered recurrent CeMV mortalities, which may have been exacerbated by the high and immunotoxic level of PCB exposure. Without significant mitigation, PCBs will continue to drive population declines or suppress population recovery in Europe for many decades to come. Measures to significantly reduce inputs of PCBs into the marine environment from terrestrial and other sources are urgently needed. Further studies are also needed to better assess PCB exposure and quantify toxic effects in marine apex predator populations in Europe. Finally, the potential impact of PCB bioaccumulation in marine ecosystems may extend beyond European waters, particularly in globally distributed marine apex predators such as KWs, false killer whales ( Pseudorca crassidens) and great white sharks ( Carcharodon carcharias).

Methods

Between January 1990 and December 2012, HPs (n = 706), SDs (n = 220); BNDs (n = 131) and KWs (n = 24) in NE Atlantic and Mediterranean Sea regions of Europe were necropsied (HP n = 706; SD n = 119; BND n = 93; KW n = 9) or biopsied (SD n = 101; BND n = 38; KW n = 15) for skin and blubber samples using standardised methodologies5,9.

Necropsies of stranded cetaceans (n = 929)

A total of 929 cetaceans were sampled or necropsied after stranding on a beach or being found dead at sea. These comprised 706 HPs; 121 SDs 93 BNDs and 9 KWs. In the UK, stranded or bycaught HPs (n = 706), BNDs (n = 38) and KWs (n = 7) were necropsied using methods based on a standardised European necropsy protocol53. Necropsies were also conducted on stranded SDs (n = 119) from western Mediterranean, BNDs from Galicia, Spain (n = 11) and Portugal (n = 5) and a single KW stranded in the Strait of Gibraltar, Spain using similar methods. Wherever possible, stranded cetaceans in fresh or slight decomposition were prioritized for necropsy to limit decomposition of tissue samples including blubber. Fresh or slightly decomposed carcasses comprised 802/929 (86.3%) of all necropsies and included 660 HPs; 103 SDs; 33 BNDs and 6 KWs. Moderately decomposed carcasses accounted for 72/929 (7.75%) of necropsied carcasses including 37 HPs; 21 BNDs; 11 SDs; and 3 KWs. Only 18/929 (1.94%) carcasses were in advanced decomposition comprised 8 HPs; 5 BNDs and 5 SDs. State of decomposition could not be determined for 37/929 (3.98%) carcasses comprising 34 BNDs; 2 SDs and 1 HPs. Sex was determined on necropsy. Sex was not recorded or could not be determined (e.g. due to loss of gonads from scavenging animals) for 65 SDs and 6 BNDs. Causes of death in UK-stranded animals were determined by specific and established diagnostic criteria5. Additional chlorobiphenyl congener and other data were included from a single KW that stranded at Roches Point, Cork harbour, Ireland and was sampled on 8 th July 200112.

Blubber samples from biopsied cetaceans (n = 152)

Blubber biopsies of free-living SDs from the western Mediterranean Sea (n = 101), BNDs from the Gulf of Cadiz (n = 11), Strait of Gibraltar (n = 11) and northern Adriatic Sea (n = 6) and skin/blubber biopsies of KWs from Canary Islands (n = 8) and Strait of Gibraltar (n = 7) were obtained using a range of standardised techniques including use of a cross-bow54. For BNDs and SDs in the western Mediterranean Sea, the skin and blubber tissue biopsy was excised from bow-riding dolphins using a sterile biopsy dart of the butterfly valve type, shot with a spear gun or a compressed air pistol from a boat, a non-destructive technique commonly used in cetacean research54. Darts were aimed at the region posterior to the dorsal fin. The precise age or sex of the individual samples was unknown. The samples collected contained about 0.8 g of blubber. Once collected, the skin and blubber biopsy samples were wrapped in aluminum foil and preserved at −20 or −80C until analysis. Sex of biopsied animals was determined using molecular techniques55. Additional chlorobiphenyl congener and other data were included from BNDs (n = 8) biopsied in the Shannon estuary, Ireland in September 200056.

Assessment of sexual maturity in cetaceans

Sexual maturity was determined in necropsied animals by analysis of gonadal material57. For those individuals where sexual maturity status data based on gonadal assessments were unavailable, published data on age and length at both sexual and physical maturity were used as criteria for assessing maturity status - BNDs58, SDs59,60 and KWs61. Animals assessed as sexually immature comprised HPs (n = 413), SDs (n = 62), BNDs (n = 35) and KWs (n = 2). Animals assessed as sexually mature comprised HPs (n = 280), SDs (n = 59), BNDs (n = 41) and KWs (n = 21). Sexual maturity status could not be determined for HPs (n = 13), SDs (n = 99), BNDs (n = 55) and KWs (n = 1).

Determination of ∑PCB in blubber samples (mg/kg lipid)

Two different laboratories conducted chemical determination of PCB concentrations in 1073/1081 (99.3%) blubber samples. The Centre for Environment, Fisheries and Aquaculture Science (Cefas) in Lowestoft, UK conducted analyses of ∑PCB for 706 HPs, 82 BNDs and 24 KWs stranded or biopsied in the NE Atlantic or central Mediterranean Sea between 1990 and 2012. The Department of Animal Biology and Biodiversity Research Institute (IRBio), University of Barcelona, in Barcelona, Spain analysed 220 SDs and 41 BNDs, predominantly from the western Mediterranean Sea. A third laboratory, the Marine Institute, in Galway, Ireland examined blubber biopsies from 8 BNDs from the Shannon estuary, Ireland56.

Cefas data

The blubber samples at the Cefas lab were analysed for 25 individual chlorobiphenyl congeners (IUPAC numbers: 18, 28, 31, 44, 47, 49, 52, 66, 101, 105, 110, 118, 128, 138, 141, 149, 151, 153, 156, 158, 170, 180, 183, 187, 194) (sum25CBs mg/kg lipid) using internationally standardised methodology4,5. After thawing, the homogenised subsamples (~5g) were dried by mixing with anhydrous sodium sulphate and storing in a freezer for a minimum of 12 hours prior to further analysis. The samples were subjected to Soxhlet extraction using of acetone: n-hexane 1:1 ( v:v) for 5.5 hours. The total extractable lipid content was determined gravimetrically after evaporation of the solvent from an aliquot of the uncleaned extract. Depending on the lipid content of the samples, varying volumes of the biota extracts were cleaned to have ~50 mg of lipid in the samples for PCB analysis. For marine mammal blubber samples, this was usually 1mL out of the 100mL extract.

For clean-up and PCB analyses, an aliquot of the blubber extracts were cleaned up and fractionated using alumina (5% deactivated) and silica (3% deactivated) columns, respectively. The final GC-ready fractions were spiked with PCB53 internal standard and made up to a final volume of 1 ml. PCB concentrations were determined with an Agilent 6890 GC with μECD. The separation of analytes was performed on a 50.0 m × 200 μm, 0.33-μm-film-thickness DB-5 capillary column (J&W). The carrier and ECD make-up gas were hydrogen (32.2 psi constant pressure, initial velocity 50 cm/s) and argon/methane (95:5), respectively. The initial oven temperature was 90 °C, held for 2.00min, then increased to 165 °C at 15 °C/min, to 285 °C at 2 °C/min and finally held for 23 min. The injector temperature and detector temperature was 270 °C and 300 °C, respectively. A 1-μl extract was injected in splitless mode with a purge time of 2 min. The PCB standard solutions contained the following 27 compounds in iso-octane: Hexachlorobenzene; p,p'-DDE; CB101; CB105; CB110; CB118; CB128; CB138; CB141; CB149; CB151; CB153; CB156; CB158; CB170; CB18; CB180; CB183; CB187; CB194; CB28; CB31; CB44; CB47; CB49; CB52; CB66; together with the internal standard CB53. Quantitation was performed using internal standards and 7 calibration levels (range 0.5-100ng/ml).

For Quality Assurance and Quality Control the Cefas laboratory participates biannually in proficiency testing scheme Quasimeme (Quality Assurance of Information for Marine Environmental Monitoring in Europe) as external quality assurance. All analyses were carried out under full analytical quality control procedures that included the analysis of certified reference material(s) and a blank sample with every batch of 10 samples analysed so that the day-to-day performance of the methods could be assessed. If levels of target analytes in the samples were outside of the range of the instrument calibration, extracts were diluted to be within range and re-analysed. Reference material used was BCR349 (cod liver oil; European Bureau of Community reference), which has been used in the Cefas lab since 1993. The results obtained for the reference materials were plotted as Shewhart quality control charts for each compound determined. The charts had previously been created by the repeated analysis of the above certified reference materials in the Cefas Lowestoft Laboratory using the North West Analytical Quality Analyst software™ (Northwest Analytical Inc., USA). Warning and control limits had been defined for the charts as 2σ and 3σ - 2x and 3x the standard deviation from the mean for each compound. The results obtained for all samples analysed were accepted as valid as the results for the certified reference materials were within the limits set by the control charts.

IRBio data

Lipid weight concentrations (mg/kg lipid) of 23 individual chlorobiphenyl congeners (IUPAC numbers: 95, 101, 136, 110, 151, 144, 149, 118, 153, 141, 138, 187, 183, 128, 174, 177, 202, 171, 180, 170, 201, 203 and 195) (sum23CBs mg/kg lipid) were generated for 220 SDs and 41 BNDs from western Mediterranean Sea using internationally standardised methodology42,62. Approximately 1 g of tissue was ground with anhydrous sodium sulphate using a mortar. The mixture was extracted with n-hexane for 4 h in a Soxhlet apparatus with a capacity of 125 ml. The solution obtained was concentrated to 40 ml. A portion of this extract (10 ml) was used to gravimetrically determine the quantity of extractable fat per gram of blubber. A further quantity was mixed with sulphuric acid for the purpose of cleaning it and the resulting extract was concentrated to 1 ml and centrifuged for five minutes.

A sample volume of 0.5 μL was injected in splitless mode (1 min splitless vent time) into a Thermo Scientific ITQ 900 GC/MS system equipped with a 30-m DB-5 MS (95% metylsilicone and 5% phenyl) fused-silica capillary column with an ID of 0.25 mm and a film thickness of 0.25 μm, with helium as the carrier gas at constant flow of 1 ml min −1. Injection port and transfer line temperatures were 270 and 300 °C, respectively. The oven temperature program was as follows: 60 °C for 1 min, an increase to 315 °C at 6 °C min −1 and a final hold of 20 min. Source temperature was 200 °C. Mass spectrometry was performed in electron impact mode. Full-scan spectra were acquired over the m:z range 50-550.

The total PCB concentration (tPCB) was calculated as the sum of the 23 congeners known as IUPAC# 95, 101, 136, 110, 151, 144, 149, 118, 153, 141, 138, 187, 183, 128, 174, 177, 202, 171, 180, 170, 201, 203 and 195. Identification and quantification of the individual compounds were performed by comparison with external reference standards calibrated with a 6-point calibration curve encompassing the entire concentration range. The detection limits were between 0.1 to 1 μg kg −1 for the PCBs standards. Analyses were performed in a series of 10 samples and 1 blank. The recoveries of the PCBs were calculated by adding known amounts of a standard to 12 homogenised replicates of the same sample; recovery levels ranged from 82-101%.

Marine Institute (Galway) data

The Marine Institute, in Galway, Ireland examined blubber biopsies collected in 2000 from 8 BNDs from the Shannon estuary, Ireland [ see 56 for Methods].

Data integration

A conversion factor [0.9] was generated to integrate the different sets of PCB data ( Cefas, IRBio and Marine Institute) using a statistical analysis of the 13 CB congeners common to both methods [i.e. sum25CBs = sum18CBs*0.9]. The combined and converged PCB data was referred to as "sum18-25CBs (mg/kg lipid)" or \xAD\xF4PCB ( Supplementary Dataset).

Spatial and temporal trends in ∑PCB exposure

To assess the temporal trends in HP and SD data we fitted a Generalised Additive Model (GAM) to the data using the R package mgcv 63. We smoothed the data using thin plate regression splines and the degree of smoothing was determined by the integrated generalised cross validation function64. The smoothing parameter gamma was set at 1.4 for HPs and set at 2.0 for SDs. To assess the spatial distribution of HP and SD data we used ∑PCB data from 1996-2012 showing spatially smoothed mean values for the ∑PCB data. This period was chosen to maximise data most representing current level of ∑PCB exposure in these species based on their temporal trends. Figures showing the spatial distribution of ∑PCBs (lipid weight) were produced in Esri ArcMap 10.1 ( www.esri.com). Data points are shown along with local averages. These averages were calculated by kernel smoothing using a polynomial order 5 kernel with power = 0, ridge parameter = 50 and bandwidth based on the spatial distribution of the observations for each species: bottlenose dolphin 0.75 degrees; harbour porpoise 0.5 degrees; killer whale 1.2 degrees; striped dolphin 0.5 degrees.

Comparison of ∑PCBs concentrations in relation to marine mammal toxicity thresholds

Two PCB toxicity thresholds were used in this study. A lower PCB toxicity threshold was used for the onset of physiological endpoints in marine mammals of 17 mg/kg lipid weight (lw) (as Aroclor 1254)7, that was calculated to be equivalent to 9.0 mg/kg lw (as ∑PCB) in this study. A higher PCB toxicity threshold, the highest reported in marine mammal toxicology studies, of 77 mg/kg lw (as Clophen 50) for reproductive impairment in Baltic ringed seals ( Pusa hispida)6 was calculated to be equivalent to 41 mg/kg lw (as ∑PCB) in this study. Differences for sex and cause of death in mean ∑PCBs concentrations in HPs only were investigated using univariate analysis of variance (ANOVA). Since only 4 months of ∑PCB data was available for HPs and SDs in 1990, some statistical analyses were conducted from 1991 onwards for these two species. All ∑PCB data were natural logarithm transformed (ln) prior to statistical analysis to satisfy the requirement for the residuals of ∑PCB data to be normally distributed.

We determined long-term spatial and temporal trends in ∑PCB in two cetacean data sets being UK-stranded or bycaught harbour porpoises (HPs) (n = 706) from 1990-2012 and stranded or biopsied striped dolphins (SDs) (n = 220) from 1990-2009 in the western Mediterranean Sea. Secondly, we assessed mean, sample median and population median (predicted by the geometric mean of the sample ∑PCB data) for ∑PCB exposure in male and female HPs of all ages stranded in the UK (n = 706) and stranded/biopsied SDs (n = 220), bottlenose dolphins (BNDs) (n = 131) and killer whales KWs (n = 24) from NE Atlantic and Mediterranean waters. Since our ∑PCB data is lognormal - we can use the geometric mean (GEOMEAN) as the best estimate of the population median together with upper and lower 95% CIs10. ∑PCB concentrations in UK HPs that were "healthy" and died of acute physical trauma (control group) (n = 345) were compared to ∑PCB concentrations in HPs that died of a range of infectious diseases (case group) (n = 252). Sex differences in ∑PCB concentrations of all species were assessed for 3 subsets of animals: sexually mature individuals only; sexually immature animals only; and those individuals where sexual maturity status was undetermined. Finally, we compared mean ∑PCB concentrations between stranded and biopsied BNDs, SDs and KWs (all HPs were stranded).

Population Dynamics

We reviewed the current population dynamics data, mortality data (including bycatch) and reproductive status of the extant KW and other odontocete populations in European waters using strandings and necropsy data from this and other studies and systematic local and international observational surveys and other data on conservation status collected over the past 15-20 years (e.g. IUCN criteria)8.

Permits

The UK Cetacean Stranding Investigation Programme conducts work on UK strandings under contract to the UK Department of Environment, Food and Rural Affairs. It has appropriate licenses from the relevant authorities (Natural England, Scottish Natural Heritage and Natural Resources Wales) to allow it to collect and hold carcasses and samples from European Protected Species, in line with UK legislation enacted under the EU Habitats Directive. The blubber samples analysed at the University of Barcelona were obtained from the biological tissue bank of the University of Barcelona (BMA Tissue Bank) and originated either from biopsies or from naturally stranded individuals. In Spain, no specific permits are required to carry out research on samples stored at public institutions. The Spanish Government translates the competency for wildlife conservation to the regional governments of the various Autonomous Communities involved in this study and the latter provided the permits for attending strandings, obtaining tissue samples and using them for scientific studies. All the technicians that work on marine animal strandings from the Portuguese Wildlife Society are licensed for the capture, handling, tagging and sample collection in mainland Portugal under the Decree-Law n° 140/99 of 24th April, with new redaction given by Decree-Law n° 49/2005 of 24th February and Decree-Law n° 316/89 of 22nd September. The licenses were issued by the Institute of Nature Conservation and Forestries (Government of Portugal) every year and all blubber samples were sent to the UK with the necessary CITES certification. Biopsy sampling in Slovenia was conducted under the permit of the Slovenian Environmental Agency #35601-102/2010-4. The samples in the Shannon estuary were collected under license from the National Parks and Wildlife Service.

Additional Information

How to cite this article: Jepson, P. D. et al. PCB pollution continues to impact populations of orcas and other dolphins in European waters. Sci. Rep. 6, 18573; doi: 10.1038/srep18573 (2016).

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Acknowledgements

The research was conducted by the UK Cetacean Strandings Investigation Program (CSIP) and the Centre for Environment, Fisheries and Aquaculture Science (Cefas) under contract to the UK Department for Environment, Food and Rural Affairs (Defra) and the Devolved Governments of Scotland and Wales. Additional funding for toxicological analyses was provided by ASCOBANS under contract "SSFA2010-3" and by the Fundació Barcelona Zoo. The Gulf of Cádiz and Strait of Gibraltar samples collection were sponsored by Loro Parque Foundation, Fundación Biodiversidad, CEPSA and ECOCET Project (CGL2011-25543) and logistical support for sample sexing was provided by Laboratorio de Ecología Molecular, Estación Biológica de Doñana, CSIC (LEM-EBD). Samples from Galicia were obtained with the support of Direccion Xeral de Conservacion da Natureza-Xunta de Galicia, co-financed with European Regional Development Funds (ERDF/FEDER). S. Murphy was supported by a Marie Curie International Outgoing Fellowship within the Seventh European Community Framework Programme. R. de Stephanis and J. Giménez were supported by the Severo Ochoa Programme for Centres of Excellence in R + D + I (SEV-2012-0262). A. D. Foote was supported by a Lawski Foundation stipend.

Author information

Affiliations

1. Institute of Zoology, Zoological Society of London, Regent's Park, NW1 4RY, London, UK

Paul D. Jepson

, Rob Deaville

, Sinéad Murphy

, Andrew A. Cunningham

, Matthew W. Perkins

& Robin J. Law

2. Centre for Environment, Fisheries and Aquaculture Science, Pakefield Road, NR33 0HT, Lowestoft, UK

Jonathan L. Barber

, Jon Barry

, David L. Maxwell

, Alexandra Papachlimitzou

& Robin J. Law

3. Department of Animal Biology and Biodiversity Research Institute (IRBio), University of Barcelona, Barcelona, Spain

Àlex Aguilar

& Asunción Borrell

4. Scottish Marine Animal Stranding Scheme, SRUC Veterinary Services Drummondhill, Stratherrick Road, Inverness, IV2 4JZ, UK

Andrew Brownlow

, Nicholas J. Davison

& Mariel ten Doeschate

5. CIRCE, Conservation, Information and Research on Cetaceans, Cabeza de Manzaneda 3, 11390, Algeciras, Spain

Ruth Esteban

& Philippe Verborgh

6. Department of Conservation Biology, Estación Biológica de Doñana (EBD-CSIC), Americo Vespuccio S/N, Isla Cartuja, 42092, Sevilla, Spain

Joan Giménez

& Renaud de Stephanis

7. Cornwall Wildlife Trust Marine Strandings Network, Five Acres, Allet, TR4 9DJ, Truro, UK

Jan Loveridge

& Nick Tregenza

Contributions

P.D.J., R.D., À.A., A.B., S.M., J.B., A.B., J.B., S.B., N.D., R.E., M.F., T.G., J.G., J.L., Á.L., V.M., R.P., M.W.P., B.S., R.de.S., N.T., P.V. and A.F. assisted with collection of blubber samples and associated biological and other data. P.D.J., R.D.,. J.L.B., À.A., A.B., S.M., J.B., A.B., M.tD., D.L.M. and R.L.L. helped to analyse the data. J.L.B., À.A., A.B., D.L.M., A.P. and R.J.L. conducted chemical analysis of blubber samples. P.D.J., R.D., J.L.B., À.A., A.B., S.M., J.B., A.B., J.B., S.B., A.A.C., M.tD., N.D., R.E., M.F., A.D.F., T.G., J.G., J.L., Á.L., V.M., D.L.M., A.P., R.P., M.W.P., B.S., R.deS., N.T., P.V., A.F. and R.J.L. helped with writing and editing final manuscript.

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# data[].attributes.attachment_link.title
PCB pollution continues to impact populations of orcas and other dolphins in European waters

# data[].attributes.attachment_link.description
Organochlorine (OC) pesticides and the more persistent polychlorinated biphenyls (PCBs) have well-established dose-dependent toxicities to birds, fish and mammals in experimental studies, but the actual impact of OC pollutants on European marine top predators remains unknown. Here we show that several cetacean species have very high mean blubber PCB concentrations likely to cause population declines and suppress population recovery.

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This shows how PCBs affects orcas and other marine animals.

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This video describes the causes and effects of PCBs in killer whales.