Australasian Science: Australia's authority on science since 1938

Nature Calls

Credit: Andy Bennett

Credit: Andy Bennett

By Mylene Mariette

In a small Australian desert bird, parents talk to their eggs to warn them it’s hot outside. The unborn chicks that listened became more successful parents.

We’ve long known that in many animals, including ourselves, embryos can hear external sounds before birth. What we didn’t suspect was that birds take advantage of this to tell their embryos something about the world they are about to encounter.

In humans, mothers speak to their baby in the womb or even play music to the foetus. That’s partly inspired by some fascinating research showing that rhythmic sounds, including music and spoken languages, influence the development of the brain and how it functions. For example, human foetuses learn about familiar voices and characteristics of their native language before they are born.

What we are much less familiar with is that birds also talk to their unborn babies. Researchers have actually known for a long time that in species where the chicks leave the nest as soon as they hatch, such as chickens and ducks, mothers talk to their eggs during incubation. This helps the embryos in the egg to learn to recognise their mother’s calls so they can follow her when they hatch.

What we’ve discovered now is that what birds tell their embryos has much longer-lasting consequences than those observed at hatching; these effects last until adulthood. Furthermore, the sounds heard before birth affect not just learning and cognition but also the physical development of the young.

Our study, published in Science (http://tinyurl.com/hlhqjnx), found that when Australian zebra finches call to their eggs to warn them about hot conditions, the chicks adjust their growth rate and end up being lighter in hot nests. Following this growth strategy allows them to produce more babies when they become adults. Hearing the parent’s hot call during incubation also makes individuals prefer hotter nests to breed in once they grow up.

How did we find out about all this?

It all started a few years ago when I was making audio recordings in zebra finch nests to study acoustic communication between parents. Besides the calls partners make to talk to each other when they meet at the nest, I noticed that parents sometimes make a completely different call when they are alone in the nest incubating the eggs.

I wondered if parents could be using that special call to talk to their eggs. What could they be telling their eggs? I decided to figure this out, together with Katherine Buchanan.

We started by placing small microphones in the nest of incubating parents to find out when they produce that special “incubation call”. The birds were breeding in outdoor aviaries, where they experienced normal variations in ambient temperature. The weather in Geelong and Melbourne is notoriously variable, as we often have “four seasons in one day”. It’s generally hot in summer and hot days are common, but we often go from a maximum of 40°C one day to 23°C the next day.

After analysing over 600 hours of audio recording from the nests, it became very clear that parents only call to their eggs on hot days when the ambient temperature rises above 26°C. But they don’t call spontaneously whenever it is hot; they only call on hot days within 5 days of hatching, possibly because their embryos are not developed enough to hear them before that.

Why would zebra finch parents need to warn their embryos about the heat? Embryos cannot tell that it is hot outside because their parents keep the eggs warm at 37.5°C by incubating them.

Zebra finches, like many desert birds, are opportunistic breeders: they don’t breed during a specific season but rather at any time they can, usually after rain. And rain in the Australian arid zone is highly unpredictable; it always takes everyone by surprise.

So sometimes zebra finches breed when it’s hot, and sometimes they breed when it’s cold. Their embryos don’t know what to expect after they hatch – unless their parents tell them.

Being prepared for the specific conditions prevailing just after birth is important. Environments always vary, even for birds breeding at the same season every year, as the abundance of food and predators fluctuate.

We know mothers can adjust the development of their babies to those specific conditions. They do this by changing the size of the eggs they lay, or how much hormones, nutrients and antibodies go into the eggs.

Could this happen with sound? Could that incubation call that parents make when it’s hot also modify the development of their offspring?

To test this we did a playback experiment. Eggs were removed from their nests after laying and incubated artificially, while parents were incubating dummy eggs. In the last 5 days before hatching we played recorded calls to eggs in the incubators. Eggs heard either the incubation calls that parents do when it’s hot, or another type of call that parents do to talk to each other.

The eggs hatched in the incubators, and the chicks were then returned to the outdoor aviaries, in either hot nests in the sun or cold nests in the shade. The parents, of course, didn’t know which calls their chicks had heard in the incubators, and raised them as if nothing happened. We monitored the growth of the chicks by weighing them on an electronic scale, just like any paediatrician does.

It turned out that the chicks did pay attention to the calls they heard in the incubators. Individuals that heard the hot incubation calls gained less weight in hot nests, whereas individuals that heard the control calls did the opposite.

We were a bit puzzled by these results to start with, because we expected that the chicks that had been warned about the heat by the incubation calls would grow better in hot nests rather than worse. Usually, light nestlings have less chances of survival because they have fewer reserves. Are things a bit different when it’s hot?

Smaller bodies may be easier to cool down because of the larger surface area to volume ratio. And slowing down growth may limit cellular damage associated with growing in the heat. Could the low-growth strategy of the forewarned chicks be a good thing?

The best way to find out was to see how many babies these birds had when they became adults themselves. In animals, the number of offspring produced is a good measure of individual success because it reflects how well individuals’ genes are passed onto the next generation, and whether this strategy is likely to be maintained in the population over time.

Like the chicks that heard the incubation call, females that as chicks were heavy in cold nests or light in hot nests produced more babies as adults. And this effect was not just transient: we observed the same effect in the females’ second year of life, even though many of them were now with a different male partner.

This was not the only long-term effect of the sound heard before birth. Males that had heard the incubation calls in the egg picked hotter nests as adults when it became time to breed. This suggests that they preferred, or did not avoid, hotter microclimates within the environment.

So overall we found that being forewarned about heat by their parents’ incubation calls allowed nestlings to adopt the best growth strategy in hot weather. How did that happen?

We have no answer to this question yet, but the most likely is that hearing the call as embryos triggered a specific physiological response that changed the way nestlings then reacted to heat. The thermoregulation system of the chick, which starts developing around hatching time, is an obvious suspect, although we are also pursuing other avenues. For example, we also found that exposure to incubation calls changed the vocal behaviour of the nestlings.

While there are still many unknowns, we discovered that bird parents can direct the development of their babies by sound alone. Our study is also the first one to find a mechanism for warm-blooded animals to adjust the development of their young to temperature. This is encouraging given global warming trends.

However, we need to remember that the zebra finch is a desert-adapted species, and that the temperatures birds experienced in our experiment were within their normal range. This mechanism is less likely to be found in birds from cooler and more stable environments, and may not be enough for desert birds to cope with extreme heat. Nonetheless, studying desert species allows us to discover what strategies exist and how they work.

The zebra finch is not a random desert bird. It is one of the best-studied bird species worldwide. We are therefore in an excellent position to understand the epigenetic, physiological and neurological mechanisms underlying the effects we observed.

Furthermore, while researchers had generally assumed that songbirds could not hear before hatching, our study now opens exciting avenues for studying the effect of prenatal sound on song learning. Song learning in birds is very well studied because it shares many characteristics of language acquisition in humans.

It looks like the zebra finch still has many secrets to deliver to scientists and the public.


Mylene Mariette is a postdoctoral research fellow in the Centre for Integrative Ecology at Deakin University.