It’s easy to see why a parrot might appeal to a painter. It alights on a canvas in an eye-catching burst of exoticism. Its plumage employs the full range of the palette, from brash shrieks of crimson through bright sunshine yellows to hyacinthine blues.

No wonder that so many artists have been tempted. The list of masters who have painted this dandified creature reads like some lofty art-historical roll call. Van Eyck, Mantegna and Dörer, Titian, Rubens and Rembrandt, Courbet, Manet and Delacroix are just a few of the more illustrious portraitists of the Psittacidae family.

And now a modern-day gallery directorhas joined the long list of aficionados of these flamboyant birds (Charlemagne, Henry VIII, Catherine the Great, Wagner and Queen Victoria among them). Richard Verdi, a professor of art history and director of the Barber Institute in Birmingham, brings together his twin passions in his new show The Parrot in Art .

It’s worth buying the catalogue. It outlines the story of our 2,500 year fascination with this extravagant creature: a tale that dates back to the era of Alexander the Great, who, having conquered the Persian Empire, marched his army across the Hindu Kush and into the Punjab. From there he returned with a novel pet: a small green bird with a rose-pink collar and blue cheeks, to which he subsequently lent his moniker. It came to be known as the Alexandrine parakeet.

By Roman times, Verdi tells us, parrots had become well known in the West. Because of their ability to speak and perform, the Ancient world regarded them, he says, “as creatures capable of breaching the dividing line between nature and culture”. And, according to legend, when Julius Caesar returned triumphant from the battle of Actium, he was greeted by a parrot squawking “Ave Caesar” — proof not only of its acumen, apparently, but also of its prophetic powers.

In the Middle Ages this story was adapted to religious purposes. It was “Ave Maria” that the prescient bird had said. The parrot had clambered into an elevated emblematic role: a symbol of the Virgin for such masters as Van Eyck and Mantegna. Their images are not included (except in catalogue reproduction) in this small show, but the point is well illustrated by a beautiful 15th-century woodcut in which a parakeet nestles tenderly upon the Christ Child’s bosom, and in an early engraving by Martin Schongauer in which the bird perches impishly upon His chubby fist.

By the Renaissance the parrot had made a sideways symbolic hop. “It was a bit of a non sequitur, but the Virgin was regarded as the new Eve,” explains Verdi, and because “Ave” is Eve spelled backwards (Eva), the parrot earned itself a special place as an eyewitness to the Fall of Man in the Garden of Eden. The great Rubens in which a beady-eyed macaw ogles the apple Eve plucks is not in this show, but Dörer’s elegantly engraved rendering of the subject is.

This idiosyncratic exhibition flutters from genre to genre, following the parrot in its many roles. Here it is as a precious plaything of the aristocracy, a high-status guest at the table of the 16th-century Lord Cobham, or (in a painting by Landseer) at the top of the pecking order of Queen Victoria’s many beloved pets. It alights, a bright splash of animation, upon the sumptuous still lifes of a Dutch Golden Age, or pecks at the more spartan fare of their modern equivalent in a beautiful little canvas by William Nicholson.

For Sir Joshua Reynolds it becomes a proof of painterly skill (his pet macaw, apparently, launched an enraged attack on its painted image, which prompted the painter to remember the famous story of Zeuxis’ lost masterpiece in which the grapes looked so real that a bird flew down to peck at them). It brings the palette of such natural history painters as Edward Lear and Elizabeth Butterworth to vibrant life.

For a prim young Dutch lady of the 17th century an African grey makes a slightly bolshy companion. But in Tiepolo’s capricious portrait Young Woman with a Macaw , in which a dreamy young lovely with rosebud nipple bared fondles her scarlet pet, the parrot takes on a more salacious role — and what’s more it’s aware of it: it catches the spectator’s eye with its own wily stare. The magnificent Delacroix and Courbet canvases, in which a parrot takes on an overtly erotic part, are not included in this show. But we do see the bird as it reflects other forms of human behaviour: leaning to take a sip of wine in Jan Steen’s The Effects of Intemperance , for instance; or taking the role of the prattling preacher in a satirical Goya print; or bossing the other birds in Henry Stacey Marks’s anthropomorphic portrait of the inhabitants of London Zoo’s bird house. The parrot, it seems, lives a very colourful artistic life.

The Parrot in Art is at the Barber Institute of Fine Arts, Birmingham (0121-414 7333), until April 29