“It [the reef] wasn’t losing the capacity to produce babies," Professor Hughes said. "There just weren’t enough adults.”

More surprising, though, was a shift in species recruitment, with so-called spawning corals faring much worse than brooding ones.

Spawning corals - including Acropora genus corals such as staghorn or table ones - typically dominate the reefs in the Indo-Pacific, accounting for about 90 per cent of reef-building varieties.

Their offspring - typically sent out in a cloud of eggs and sperm that fertilise over as long as a week - fell as much as 98 per cent.

By contrast, the Pocillopora corals saw offspring numbers drop about a third. These varieties - often shaped like cauliflower - retain their eggs and fertilise internally, and produce fewer larvae that typically settle close to the mother.

One implication of the findings is that reefs may need longer than thought between bleaching events if they are to recover.

"It’s going to take at least five, more likely 10 years for the adult population to rebuild to make as many babies as they used to make," Professor Hughes said.

Unfortunately, the period between bleaching events - caused when water temperatures exceed certain thresholds, causing the corals to expel the algae that provide them with most of their food and colour - is shortening because of global warming.

While the reef has been bleached four times in the past 20 years, "it is projected by climate models to bleach twice each decade from 2035 and annually after 2044, under a business-as-usual scenario for greenhouse gas emissions", the paper said.

The distribution of species, though, to favour the brooders means the recovery may also be limited by distance. Remote reefs hard hit by bleaching, for instance, won't have as many of the Acropora larvae heading their way as in the past.

Similarly, even though the southern third of the Great Barrier Reef largely escaped damage from the bleaching events, currents typically flow the wrong way for those reefs to repopulate northern ones.

French Polynesia is an example of how brooders have taken over from previously dominant spawning corals, Professor Hughes said.

Katharina Fabricius, senior principal research scientist with the Australian Institute of Marine Science, said it was "a really important paper" that demonstrated how "severe the pressures from heat stress are for all the life stages of coral".

Another emerging threat is the rising acidification of the sea water as a result of higher atmospheric carbon dioxide levels. Young corals have been found to have a 10-fold increase in sensitivity to acidity, a shift that also threatens to undermine their ability to reproduce, Dr Fabricius said.

"We used to think that the Great Barrier Reef was this robust resilient system that couldn’t fail because it’s too big, and all the [3000] reefs are interconnected and they can rescue each other, say, after a cyclone," Professor Hughes said.

"We’re not saying it won't recover again. It will recover more slowly, and more likely to something else."