To the human ear they sound like the tinny thud of a small starter motor, but to a mother crocodile they are the plaintive calls of her egg-bound babies, saying they are about to hatch en masse and could she please make sure there are no nasty predators nearby.
The "umph, umph, umph" calls of unhatched crocodiles have been shown by scientists to be vital vocal signals that co-ordinate their entry into the world.
For the first time, researchers have shown that the pre-hatching calls of baby Nile crocodiles actually mean something to their siblings – and to their mothers. The calls serve the essential function of telling others in the nest that it is time to hatch, as well as warning their mother to protect them, said Amélie Vergne and Nicolas Mathevon of Université Jean Monnet in Saint-Etienne, France.
The behaviour may have a long history, the researchers said. Birds also produce "embryonic vocalisations" that induce parental care. Such early communication may be a shared behavioural feature of past and present members of the Archosaurs, an ancient group of reptiles now represented by modern birds and crocodiles.
The study used recordings of the sounds made by unhatched baby crocodiles in their underground nests. It demonstrated that mothers show signs of caring behaviour.
"Hatching synchrony can be of vital importance for crocodiles," said Dr Mathevon. "Indeed, most mortality occurs early in life and hatching vocalisations might well attract predators.
"Therefore, adult presence at the nest and its response to juvenile vocalisations may offer protection against potential predators. In this sense, it is important for all embryos in the nest to be ready for hatching at the same time so that they all receive adult care and protection."
The calls tell the mother crocodile to start digging up the nest, according to the study published in the journal Current Biology, which was based on a "playback" experiment.
Crocodilians were known to make sounds within the egg shortly before hatching, the researchers said. To find out what those calls might mean in the new study, the researchers divided crocodile eggs that were due to hatch within 10 days into three groups. One of those groups was played recordings of pre-hatching calls, one was played recordings of noise, and the last was left in silence until they hatched.
The eggs played the pre-hatch sounds more often answered back, they report, and many moved. All of the eggs in the pre-hatch group hatched during the playback or within 10 minutes of it. Whereas only once did the eggs hearing general noise hatch. The rest hatched at least five hours after the last test.
The researchers then tested the mothers' responses to the calls. "In the zoo where we did the experiments, eggs were removed [from the nest] within a few days following the laying date," the researchers explained. "In spite of this, females continue to guard the nest."
At the end of the incubation period, the researchers hid a loudspeaker underground near the empty nest. They then played pre-hatching calls interspersed with noise to 10 mothers. The adults more often turned their heads or moved after egg sounds than after noise, they showed, and eight of the mothers responded to the recorded calls by digging.
The same scientists have previously analysed 400 calls made by 10 young crocodiles during their first four days after hatching. They found that the calls have a "complex acoustic structure", but individual baby crocodiles do not appear to have distinctive calls – so that mothers are unlikely to recognise the calls of their own young compared to the calls of another's offspring.
It is only relatively recently that scientists have confirmed that crocodiles engage in fairly extensive maternal care. It was originally thought that they simply laid their eggs and did not get involved in either protecting them or the hatchlings.