Many owners struggle to teach their dogs to sit, fetch or even bark on command, but John Pilley, a retired psychiatrist, taught his border collie to understand more than 1,000 nouns, a feat that earned them both worldwide recognition.

In 2004, Mr Pilley bought a black-and-white border collie he named Chaser.

For three years, Mr Pilley trained her for four to five hours a day. He showed her an object, said its name up to 40 times, then hid it and asked her to find it.

He used 800 cloth animal toys, 116 balls, 26 Frisbees and an assortment of plastic items to ultimately teach Chaser 1,022 nouns.

Chaser died on Tuesday at 15. She had been living with Mr Pilley’s wife, Sally, and their daughter Robin in Spartanburg, South Carolina. Mr Pilley died last year at 89.

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Another daughter, Pilley ​Bianchi, said on Saturday that Chaser had been in declining health in recent weeks.

“The vet really determined that she died of natural causes,” Ms Bianchi said. “She went down very quickly.”

Ms Bianchi, who helped her father train Chaser, said the dog was buried in the backyard with the family’s other beloved dogs and with some of her father’s ashes.

“What we would really like people to understand about Chaser is that she is not unique,” Ms Bianchi said.

“It’s the way she was taught that is unique. We believed that my father tapped into something that was very simple: he taught Chaser a concept which he believed worked infinitely greater than learning a hundred behaviours.”

Ms Bianchi said her father’s experiment was “uncharted territory” in animal cognition research, pointing to news media coverage calling Chaser “the world’s smartest dog”.

“Her language learning is very high-level, powerful science,” she said.

Chaser understood that words have independent meaning and understood common nouns as well as proper nouns, Ms Bianchi said.

Greg Nelson, a veterinarian at Central Veterinary Associates in Valley Stream, New York, said humans were learning that animals have a deeper understanding of the world around them.

“People have always been under the belief that animals respond to commands based on a rewards system,” he said.

“Learn limited commands and tricks, then get a treat.” But “they do have a language among themselves, spoken and unspoken,” he added.