LONDON - Disturbing evidence that honeybees are in terminal decline has emerged from the United States where, for the fourth year in a row, more than a third of colonies have failed to survive the winter.

The decline of the country's estimated 2.4 million beehives began in 2006 when a phenomenon, dubbed colony collapse disorder, led to the disappearance of hundreds of thousands of colonies.

Since then, more than three million colonies in the US and billions of honeybees worldwide have died and scientists are no nearer to knowing what is causing the catastrophic fall in numbers.

The number of managed honeybee colonies in the US fell by 33.8 per cent last winter, according to the annual survey by the Apiary Inspectors of America and the US Government's Agricultural Research Service (ARS).

The collapse in the global honeybee population is a major threat to crops. It is estimated a third of everything we eat depends upon honeybee pollination, which means bees contribute about $54.6 billion to the global economy.

Potential causes range from parasites to viral and bacterial infections, pesticides and poor nutrition stemming from intensive farming methods.

The disappearance of so many colonies has also been dubbed "Marie Celeste syndrome" because of the absence of dead bees in many of the empty hives.

US scientists have found 121 different pesticides in samples of bees, wax and pollen, lending credence to the notion pesticides are a key problem.

"We believe that some subtle interactions between nutrition, pesticide exposure and other stressors are converging to kill colonies," said Jeffery Pettis of the ARS.

A global review of honeybee deaths by the World Organisation for Animal Health reported there was no single cause, but the "irresponsible use" of pesticides may have damaged bee health.

Why bees matter

Flowering plants require insects for pollination. The most effective is the honeybee, which pollinates 90 commercial crops worldwide.

As well as most fruits and vegetables - including apples, oranges, strawberries, onions and carrots - they pollinate nuts, sunflowers and oil-seed rape. Coffee, soya beans, clovers and even cotton are all dependent on honeybee pollination to increase yields.

In Britain alone, honeybee pollination is valued at £200 million ($420 million). Mankind has been managing and transporting bees for centuries to pollinate food and produce honey.

Their extinction would mean not only a colourless, meatless diet of cereals and rice, and cottonless clothes, but a collapse of the food chain that sustains wild birds and animals.