Is it finally time to stop keeping orcas in captivity?
For the last few years there has been a torrent of stories of captive orcas suffering severe health problems, and in some cases attacking and even killing their trainers.
Many of these stories have focused on an orca called Tilikum, who lives at SeaWorld Orlando in Florida. Tilikum has been involved in three deaths during his time in captivity.
SeaWorld has now announced that Tilikum's health appears to be deteriorating, possibly due to a bacterial infection in his lungs.
In response, conservation groups are once again calling for an end to the practice of keeping orcas, and other large marine mammals, in captivity. Are they right?
Captive orcas have long been a controversial subject, but an incident in 2010 dragged them into the limelight.
In front of a crowd of visitors, Tilikum dragged his trainer Dawn Brancheau under the water and killed her. He had previously been part of a group of three orcas that drowned a trainer in 1991, and in 1999 he apparently drowned a man who was trespassing in the park.
They are too large to be kept in captivity
The 2010 killing initially sparked headlines around the world expressing shock, and calling for Tilikum to be put down.
But others, especially marine mammal scientists, were not only sympathetic to Tilikum: they blamed his keepers. The 2013 documentary Blackfish argued that his violent outbursts were directly brought on by the stressful conditions of his captivity.
In line with this, several decades of observation show that orcas are not naturally violent towards humans. There are no recorded cases of a wild orca killing a human.
"In captivity, we force this artificial proximity to human beings, so the orcas do act out once in a while and kill you," says marine mammal scientist Naomi Rose of the Animal Welfare Institute in Washington, DC. "They are too large to be kept in captivity."
Orcas (Orcinus orca) are also known as killer whales, but they are actually dolphins, not whales – although both whales and dolphins belong to the same group, the cetaceans.
The practice of taking them into captivity started in the 1960s. Orcas were caught as juveniles and moved into tanks, ready to be trained to perform tricks for our entertainment.
Living in captivity is a far cry from the orcas' natural world
According to the charity Whale and Dolphin Conservation, at least 150 orcas have been taken into captivity since 1961. SeaWorld has not captured a wild orca for 35 years, instead breeding them in captivity. But elsewhere orcas are still captured: in Russia 14 have been caught since 2002.
Today 56 orcas remain in captivity, part of a total of 2,000 captive dolphins, according to the Change for Animals Foundation.
Clearly, living in captivity is a far cry from the orcas' natural world. Many researchers now argue that captivity does not come close to addressing their main needs.
To start with, consider the vastness of their natural habitat, the ocean.
They are the most social mammal on Earth
"These are animals that coordinate their movements over scales of tens of kilometres. It's difficult to replicate that in any aquarium," says conservation biologist Rob Williams at Oceans Initiative in Seattle, Washington.
Many orcas travel over 100km (62 miles) every day.
We do not quite know how far they travel in any given year, but we are starting to find out. One team tagged a group of orcas and discovered that they frequently travel all the way from the Antarctic Peninsula to Brazil and back again. At one point they travelled nonstop for 42 days and covered 9,400km (5,075 miles).
That big animals need habitats to match is obvious. What is less clear at first glance is how sociable orcas are.
All whales and dolphins are highly social, but orcas go one further. "They are the most social mammal on Earth, [and] that includes humans," says Williams.
That is because they live in multi-generational units, which live together for almost their entire lives.
We don't know if there's an occasional Romeo and Juliet romance
In particular, a male orca will never leave his mother. He goes away to mate but always returns to his pod. Orcas are the only mammals observed doing this.
What's more, each orca family can be identified by their unique calls. In other words they have a kind of culture, one that is passed down from generation to generation.
Their culture runs surprisingly deep.
Orcas live in distinct units called ecotypes, each with different habits. As well as their separate "languages" they hunt different prey. One group eats a specific salmon species, one preys on seals, and another occasionally targets humpback whale calves.
They are not fed the food they have evolved to prefer, or bred with the same type
There are ten known ecotypes, says Rose, and there might be more out there. "They tend not to breed with other ecotypes. We don't know if there's an occasional Romeo and Juliet romance, but genetically they are very different."
The ecotypes may well become more different over time. "As an animal specialises, [natural] selection then starts to act on that specialisation," says Luke Rendell of the University of St Andrews in the UK.
After analysing several orca genomes for a 2010 study, one team claimed that three orca ecotypes are distinct enough to be considered separate species. Other researchers are not convinced, but the claim highlights how different the ecotypes are.
In captivity, the ecotype an orca belongs to cannot always be taken into consideration. They are not fed the food they have evolved to prefer, or bred with the same type.
"That's the other problem with captivity, you've taken these ecotypes away from everything they know culturally and given them something barren in return," says Rose.
That degree of aggression has never been observed in the wild
Different ecotypes do not associate with each other in the wild, so it can be problematic if they are suddenly forced together.
In 1989, during a live SeaWorld show in San Diego, California, a dominant female named Kandu rammed a relatively new member of the group called Corky. Kandu tore open an artery and subsequently bled to death.
"That degree of aggression has never been observed in the wild," says Rose. "The two whales involved were from different oceans. They would never have encountered each other in the wild."
It is the diverse ecotypes that present the biggest challenge to anyone wanting to keep orcas in captivity, says Rendell. "In general it's pretty problematic… given what we know about the diversity of their behaviour in the wild. That can't happen in captivity, it just can't. We don't have the facilities."
Nevertheless, organisations that keep orcas and other large cetaceans in captivity offer several reasons why they should be allowed to continue.
Organisations like SeaWorld claim that keeping captive dolphins allows scientists and the public to learn more about them, in ways that are not possible when observing them in the wild.
They show repetitive rubbing against tanks and some have teeth worn down to a pulp
In a statement, SeaWorld said: "We provide researchers the unique advantage of animals that are trained and able to cooperate. Researchers can monitor these individuals daily over long periods of time."
But the orcas behave differently in captivity than they do in the wild, so they cannot thrive in theme park settings, according to Lori Marino, a neuroscientist by training who now advocates animal rights at the Kimmela Center for Animal Advocacy. "All of what makes life important to orcas is taken away."
This begins to show in captivity, in the form of repetitive behaviours linked to stress.
These behaviours tend to have no real purpose other than stimulating the orca's senses, says Marino.
Captive orcas do not live as long as their wild counterparts and have lower survival rates
"They show repetitive rubbing against tanks and some have teeth worn down to a pulp… That results in pain and in teeth having to be flushed out every day to avoid infection. It becomes a whole cycle of harm for these animals."
It has also been argued that keeping captive cetaceans boosts public awareness of their conservation needs.
However, Williams argues that public orca shows clearly set out to entertain first of all. "I don't have any evidence that people go home with better environmental ideas."
The median survival rate was just 6.1 years
There is now evidence to suggest the captive orcas do not live as long as their wild counterparts and have lower survival rates. According to the National Ocean and Atmospheric Administration (NOAA), wild males typically live for about 30 years but can live up to 50 or 60. Wild females usually live up to 50 but can live up to 100.
The SeaWorld website reports lower figures. They say wild male and female orcas reach average ages of 17 and 29 years respectively. These figures include those that may die in the first six months. "If a killer whale survives the first six months, a female's average life expectancy is within the range of 46 to 50 years and a male's is 30 to 38 years," SeaWorld states.
A study published in 2015 presents evidence that orcas in captivity live shorter lives than orcas in the wild. A team looked at 201 captive orcas to find that the median survival rate was just 6.1 years, with those in US facilities reaching a median of 12 years.
The authors concluded that "survival to age milestones is remarkably poorer for captive killer whales than for wild whales".
So what is the solution?
Following several years of negative press, in November 2015 one SeaWorld facility in San Diego, which holds 11 orcas, announced that it would start "phasing out" some of its circus-style shows. Instead it would present shows focusing on the orcas' "natural environment".
No longer do they want to see these caricatures leaping for our entertainment
At the time, Chris Butler-Stroud of Whale and Dolphin Conservation told BBC Radio 4 that he feared SeaWorld was "re-packaging" the show to repair their public image.
"They talk about natural setting, but we're still talking about a concrete tank," Butler-Stroud said. "People care about these creatures but they don't have to see them in tanks… No longer do they want to see these caricatures leaping for our entertainment."
Similarly, Marino says the announcement was "smoke and mirrors", because the orcas' lives will remain highly artificial. "Even if there was a real earnest desire to do something for these animals, in order for them to have better welfare they would have to be in a sanctuary where the priority is not ticket sales or entertainment, but their welfare."
It might seem that the simplest solution would be to return captive cetaceans to the ocean. But in practice this is fraught with difficulty.
The 1993 film Free Willy told the story of a boy trying to free a captive orca. The orca was "played" by a captive orca called Keiko.
Keiko was later returned to the wild, but he did not reintegrate into orca society. In a 2009 account of the reintroduction, researchers stated: "Keiko's release to the wild was not successful, though physically unrestricted and free to leave, he kept returning to his caretakers for food and company."
Keiko eventually died from pneumonia just a year after he was released.
However, this story does not mean reintroduction is entirely impossible.
In 2002, an orca called Springer was taken into captivity for her own welfare, after being found alone at sea. She was kept in a sea pen and fed the wild salmon that she was used to eating.
A few months later she was successfully released into her own family pod. In 2013, she was even observed with a calf of her own.
The reason her release was so successful was that she was only kept captive for a short time, says Rendell. "She was able to be reintroduced in an appropriate social context. Keiko wasn't."
They cannot behave in the natural ways they have evolved
Taking a cue from Springer's story, there are now efforts underway to create sea pen sanctuaries for orcas that have lived most or all of their lives in captivity. But this will take time.
"The point is that however this is done, it has to be done right," says Marino. "You can't just throw a rope across a cove and dump the animal in there. It's going to take time and a lot of expertise."
There is also a limit to what we can do for orcas that have spent most of their lives in tanks.
Regardless of whether they were born into captivity and know nothing different, or were caught when they are young, these orcas cannot live the way their wild counterparts do. "They cannot behave in the natural ways they have evolved," says Rose.