Culum Brown was five years old when he first considered that humans may not be the only intelligent animal species on the planet.
The light-bulb moment came to him, he says, when he was feeding his pet fish.
The young Brown noticed that the fish would every day gather on the same side of the tank in anticipation of the flakes of food.
It got him thinking a couple of years later about whether they could actually recognise who was feeding them. By the time he was in his early teens, he was into snorkelling and scuba diving and watching fish do all kinds of "cool stuff".
It cemented a life long pursuit investigating the smarts of fish and Brown's findings would probably surprise many.
"There's virtually nothing a fish can't do," Brown, an associate professor at Macquarie University's biology department says. "They recognise individuals, they preferentially associate with them, they deliberately manipulate individuals, they can cooperate, they show processes of reconciliation and all sorts of things, so basically everything you might find in primates you'll find in fish."
The questions of animal intelligence and related theories on sentience or consciousness have been probed and prodded by scientists and philosophers for centuries, with each new generation of minds seemingly devising alternative theories.
When looking at intelligence researchers examine how animals use cognitive abilities such as thinking, acquiring knowledge, sensory perception, memory, individual recognition and language, while sentience, or consciousness, deals more with how animals perceive what is around them and what they feel or think.
Research into these topics has gone through many stages, both humane and brutally inhumane. Rene Descartes's 17th-century teachings influenced Western beliefs for generations. The French philosopher and vivisectionist decried animals as lesser beings, or automatons, that lacked minds and souls and were not capable of reasoning. Which might explain his predilection for dissecting live animals. But Charles Darwin, whose anecdotal approach is regarded as the beginning of contemporary studies, argued that the mental powers of animals and humans differed only in "degree, not in kind" and attributed emotions to many species.
Australian philosopher Peter Singer's landmark 1975 book Animal Liberation really helped bring such concepts into the public consciousness and formed the foundations of the animal rights movement.
Kanzi is a chimpanzee that can reportedly communicate using symbols. Photo: greatapetrust.org
For much of the 20th century researchers explored the possible intelligence in primates, as the species most closely related to humans. A number of high-profile and controversial studies took place where researchers tried to prove intelligence by attempting to communicate with primates kept at research facilities. These included Kanzi, a bonobo that can reportedly communicate by using lexigrams (symbols representing words); Koko, a gorilla which uses sign language, and Ayumu, a chimpanzee that exhibits an amazing memory (it is shown the numbers one to nine on the computer screen, and given just a fraction of a second to remember their random location. The chimpanzee can tap the numbers in the correct order).
But Brown says how closely an animal is related to humans is not "in in any way a valid measure of intelligence".
"You shouldn't even have an expectation that because things are closely related to humans that they're going to be more intelligent than others," Brown says.
"Our emphasis has now shifted to understanding what are the environments or contexts that may lead to the rise of cognition more generally, so things like active foraging , [where] you go out and actually look for food, if foods are only found in particular locations at particular times and you have to solve particular problems in order to access it then those things are likely to increase intelligence generally."
Bradley Smith, a leading researcher in the behaviour of dingoes based at Central Queensland University agrees.
"Back in the 1960s we saw humans as up here and animals down there and we were the higher order species," Smith says. "But now as more research and more funding is available, and more technology and the ability to actually observe and do research on these animals, we've worked out that they are much more complex, much more intelligent, much more sentient than we ever really thought they were."
But that raises the question of where instinct ends and reasoning begins.
"I think of instinct as programmed behaviour that you have no conscious control over or thought about. You just do it," says Smith. "I think social learning, learning from watching others, that's a cognitive skill. That's not instinct, that's higher order thinking where you're making decisions and thoughts in your mind."
Smith points to his studies of dingoes, which are regarded as pests in farming regions because of attacks on livestock, that show them as "highly intelligent and highly sentient".
He says there were many examples of social learning in dingo packs where older members that have either been sick or seen other members die after eating baited meat, not only avoid baits in future but teach younger members to do the same.
"They have feelings, they have families, they're just trying to go about their lives," he says.
Smith with dingo pups. Photo: Red Collins
However, as research has delved deeper into exploring what animals were capable of, some have warned about the influence of anthropomorphism – that is, reading human traits in animals' behaviours.
In 2014, Copenhagen Zoo was the centre of a fierce backlash when it killed an 18-month-old giraffe Marius with a bolt gun and then dissected the body in public and fed it to lions.
The zoo argued that it had to prevent the animal becoming an adult because of rules discouraging the inbreeding between giraffes. It was supported by Peter Sandoee, a professor of bioethics at the University of Copenhagen, who criticised the reaction, which included death threats to zoo employees, for being the "Disneyfication" of animals.
"You take this very romantic image of animals as people with fur or feathers," Sandoee told the media. "Animals are viewed as a type of citizen, with the implication that they should be treated on par with fellow human beings."
Marius the giraffe in Copenhagen Zoo. Photo: Reuters/Scanpix Denmark
The Gorilla Foundation in the United States also opened themselves to ridicule when they released a statement last year that Koko, after being told of the death of Robin Williams, who she had spent an afternoon with a decade earlier, became "quiet and looked very thoughtful" and "at the end of the day ... became very sombre, with her head bowed and her lip quivering".
Williams with Koko. Photo: koko.org
Tiffani Howell, who has a PHD in psychology from Monash University, says "it's really hard to measure things like awareness".
"Are you defining awareness as human consciousness? Humans are very aware of the fact that we have a past and a future so we can think and we can plan based on memories and based on things that have happened to us previously.
"Can animals do that? I don't think there is any way to know for sure. There's been a lot of studies looking at intention and planning and it looks as though some great apes can do some of that and crows and ravens can do some of that but to what extent that means they are conscious the way that humans are, I think that's really, really hard to measure because they don't have [human] language."
The importance of determining whether animals have awareness has significance for the welfare of those animals, especially in livestock industries. Why should humans care about how cattle, sheep, pigs or chickens are treated if as Descartes argued, they don't have any emotions or feel pain?
Professor Paul Hemsworth, the director of Melbourne University's Animal Welfare Science Centre, which conducts extensive research into the welfare of animals in primary industries, has no doubt that animals have emotions.
"I think most biologists will assume that when we talk about vertebrates, they have the ability to express emotions," Hemsworth says.
But Hemsworth believes it is a step too far to say livestock at an abattoir or a pet on its way to a pound's euthanasia room, can sense their fate. The responses of animals in such situations such as shaking, vocalising and reluctance to move generates passionate responses by advocates but Hemsworth says the animals are reacting to physical settings and cues.
"I think it is [humanising them] and I think you have to be really careful," Hemsworth said.
"Let's take the abattoir situation. If the animals are being handled quietly and calmly and the animals are moving well, those animals will move right up to the point of being stunned before they're slaughtered.
"If the handling is aversive, [where there is] rough handling, the animals are vocalising so there are alarm vocalisations that are alerting animals behind them to the fact that there may be danger ahead, they might be releasing pheromones – chemical signals in their urine and saliva – that again indicate alarm so animals following are likely to show aversion to that situation, people might just interpret that as they know their fate.
"Animals are very good at communicating with each other especially the social animals and there's very subtle signals that they use and I think the abattoir is a very good example where animals can alert other animals to some difficulty ahead."
However, Brown claims that the continuing debate about whether fish are intelligent and feel pain has led to animal welfare concerns ending "at the water line".
"You want to minimise stress and pain and discomfort to the animals [but] that kind of thing does not exist in fisheries and there's absolutely no scientific reason for that to be the case," Brown says.
"People don't expect fish to respond to pain. They don't really care about welfare issues because they have this lower expectation of fish intelligence but everything that we've done with fishes so far and even sharks suggests that there's really very little difference amongst vertebrates generally and if you're going to treat one vertebrate one way then you really ought to treat them all the same way."
Culum Brown says fish have feelings too. Photo: Quentin Jones
Another characteristic often associated with intelligence in higher order animals such as elephants, dolphins and primates is the recognition of death. Rob Appleby, from Griffith University's Environmental Futures Research Institute, was on one of his regular expeditions on Fraser Island to observe the local dingoes and their often misinterpreted and maligned behaviour when he came across a mother dingo and her pups, one of which was in a great deal of distress and was convulsing.
He suspected that it may have been bitten by a snake, but it was the reaction of the pup's family members during the following days that really intrigued him. It took up to 30 minutes for the pup to die, during which time, the mother dingo and every sibling interacted with it, from pawing and sniffing and whimpering.
Later the mother dingo seemingly protected the body of the pup by picking it up in its mouth and repeatedly moving it to keep it close to the family.
"This is the first time that's its ever been observed in a canid [a family of animals that include wolves, jackals, foxes and domestic dogs] that we're aware of and it's certainly at least seemed to match some of the descriptions of the transport of deceased animals by species that we do ordinarily equate as being very intelligent," says Appleby, who does not know what eventually happened to the body despite a thorough search of the area.
"We tried to think of everything we could think of that was an explanation. The most logical competing hypothesis is that it was a source of food and she was simply moving it around to protect it, but my experience with dingoes on the island is that they don't tend to cache food all that often. They will do it but usually caching involves some sort of burial ... and my experience is that in that circumstance it probably would have occurred reasonably rapidly."
Rob Appleby taking video of dingoes on Fraser Island. Photo: Brad Smith
David Dowe, who is an associate professor in artificial intelligence and information technology at Monash University, is attempting to develop a test which could measure the intelligence of animals. He, and colleagues, devised an Anytime Universal Intelligence Test, which he says is "linguistically independent" and "based on the principles of information theory".
Up to now it has only been used on humans and computers, but Dowe, having seen the potential in cases such as Chaser, a border collie that can understand 1000 words, wants to expand the testing to animals.
"Whenever we try and communicate with non-human species it's seems to always about them learning our language. We don't learn their language. It's a bit one-sided really," Dowe says.
"What we can do is set exercises of varying difficulty and if you're doing well, we can ramp up the difficulty."
"One problem we have though is that the test that you set for an ant or a mollusc might be different to what you might set for a giraffe or an elephant. There are going to be interface issues but ideally we'd like to be able to set the same test in some sense for an ant as for a whale."
"I think there are some very intelligent non-humans and we have to be open to that. Our tests are just going to attempt to formalise it."
Smith, who has conducted several observational studies on dingoes, one of which he says showed a dingo moving a table around as a tool to reach elevated items, and Brown say the use of MRI scans to show brain activity in response to stimuli, was becoming increasingly important as the way of future research.
"There's only so much we can do with behaviour. We can give them problem solving tasks and can observe them in different scenarios but we're wanting to now delve a bit deeper into that kind of stuff , and one way that's non-invasive is to do MRI and you can see what parts of the brain activate ... which is taking it to a new level," Smith says.
"Of course we will never actually know what animals are thinking ... just because the same part of the brain is activating [and] the same chemicals might be released in an animal doesn't necessarily mean it's the same as a human."
The increasing understanding of the cognition of non-human life forms sparks a set of ethical questions regarding the ways humans continue to interact with animals. There have been several cases during the past 12 months that have examined what rights should be applied to animals.
Animals, in many jurisdictions including Australia, are regarded as the property of the owner and therefore have no rights. It is a perception that The Non-Human Animal Rights Project has taken the lead in fighting to change in America.
Emmanuel Giuffre, the legal counsel for Australian lobby group, Voiceless: The Animal Protection Institute, says a common misconception was that by giving animals legal rights, people were trying to treat animals as humans. He said this was not correct and such a move would simply provide basic rights and protection, such as allowing animals freedom from "wrongful captivity" and being subjected to invasive research.
Giuffre says "while it is the same principle that applies to humans, it doesn't necessarily mean that apes should then go and roam the streets" but rather animals "would then go to a sanctuary that resembles as closely as possible to their natural environment".
The Oregon Supreme Court in 2014, passed a ruling in a case of animal abuse, where a man was convicted of starving 20 horses and goats on his property, that each animal could be seen as a legal "victim" which meant that the defendant Arnold Nix could be charged with 20 counts of animal neglect rather than just one. While animals would still be regarded as property, the ruling strengthened the intervention and prosecution of animal crimes.
However, the New York appeals court ruled that the owner of a chimpanzee named Tommy was not obligated to release it from a cage in which it was kept, which an animal rights group, which wanted it transferred to a sanctuary, claimed was unlawful detention. The three judge ruling stated: that chimpanzees were intelligent but could not take on the legal implications of personhood, because "unlike human beings, chimpanzees cannot bear any legal duties, submit to societal responsibilities or be held legally accountable for their actions".
"In our view, it is this incapability to bear any legal responsibilities and societal duties that renders it inappropriate to confer upon chimpanzees the legal rights – such as the fundamental right to liberty protected by the writ of habeas corpus – that have been afforded to human beings."
There is also the case of Sandra, an orangutan kept in a Buenos Aires' zoo, that is making slow progress through the Argentinian courts with her lawyers arguing that she should be moved to a sanctuary.
Appleby says the uproar over perceived wrongs directed at animals such as whaling, annual mass killings of dolphins in Japan and increasing awareness about species being pushed to extinction, show that people's perceptions were changing as research finds traits that were once thought to only be human.
"It's that recognition of sentience, that recognition of emotion and intelligence that I think is having people start to question how we treat them and wanting to treat them better," Appleby says.
