Serenading embryos with weather forecasts

Zebra finches tweet and twitter while brooding their eggs¹.  Picture yourself, sitting still and warming a clutch of eggs -- hour-after-hour, day-after-day, waiting for the hatch. 

Maybe the finches are humming out of boredom?

Research has shown that for many species, nest calling is important. Incubating birds not only converse with their mates, but also talk to their egg-bound developing embryos^2,3. In several cases, such embryo serenades can imprint hatchlings on parental calls. 

Even unnatural sounds delivered to eggs might have consequences.  In a particularly bizarre example, Indian biologists played loud Alhaiya Bilawal (raga music) inside an egg incubator and found effects on learning and memory in the chicks that hatched later⁴.

 
What about the twittering of nest-bound zebra finches?  

After careful observations and unequivocal experiments, Mylene Mariette and Katherine Buchanan at Deakin University in Australia showed that calls of brooding finches transmit weather forecasts that reprogram the physiology of the next generation of finches¹.

Wild zebra finches thrive in central Australia where some years are hot and others are hotter. The birds are opportunistic, breeding whenever weather is favorable.

Finches nest when rains come. Over the two weeks of incubation, the birds chat to one another with tet calls and whine calls.

The tet call is a blend of frequencies, lasting about a tenth of a second, and repeated 2-3 times per second. The whine call is a warble, given once per second.
   


Late in the incubation when the other mate is away from the nest, the brooding bird uses a new vocalization, termed an incubation call - a series of 5-6 chirps at a dominant frequency of 10 KHz.




 

Brooding parents sing solo incubation calls only when:   

an egg will hatch within the next five days, and

the laboratory temperature is hot, over  26°C (79°F).

To discover whether incubation calls are linked to outdoor temperature, Mariette and Buchanan recorded calling and the daily maximum temperatures as zebra finches nested in nature, through summer solstice (December 21 in Australia) and as days shorten thereafter.


Incubation calls were given only on hot days (temperatures over 26°C). Furthermore,  the frequency of incubation calling was not correlated with seasonal changes in day length.

What could be the function of this solo incubation call? Laboratory experiments answered this question.

Mariette and Buchanan hatched two groups of eggs in lab incubators at 37.7 °C. Some developing embryos heard incubation calls while others (controls) were exposed to contact (tet and whine) calls.

As each egg hatched, the chick was popped into a nest box with finch parents who readily adopted the grafted baby bird.

Incubation calls programmed embryonic finches to become noisier and smaller birds after they hatched.  The baby birds previously exposed to incubation calls begged more avidly from their parents than controls, and the adult body size of the incubation-call group was smaller than controls who had heard only contact calls in the incubator.

Is this merely esoteric, or could there be a biological advantage in the next generations?
Mariette and Buchanan compared productivity in their two groups of hatchery-incubated birds, allowing birds from both groups to nest in hot conditions or in cooler conditions.

• When nesting temperatures were hot, the breeding birds that had been exposed to incubation calls produced more young than the controls who heard no incubation calls in the egg. 
• When nesting temperatures were cooler, the controls did better.

The overall conclusions:

• Incubation calls of brooding finches are heat-actuated, tweeted only when the temperature is high.
• To late-stage embryos, incubation calls are weather forecasts based on present temperatures.  
• Incubation calls switch developmental trajectories of the hatchlings, resulting in higher productivity if the next nesting season is likewise hot.  
• When hot seasons follow after one another, this call-actuated switch might serve as a preadaptation for climate change.  

 References: 
1. Mariette MM,  Buchanan KL, 2016, Prenatal acoustic communication programs offspring for high posthatching temperatures in a songbird. Science 353:812-814.
2. Bolhuis JJ, 1991 Mechanisms of avian imprinting: a review. Biol Rev Camb Philos Soc 66:303-345.
3. Woolf NK, Bixby JL, Capranica RR, 1976,  Prenatal experience and avian development: brief auditory stimulation accelerates the hatching of Japanese quail. Science 194:959-60.
4. Sanyai T, Kumar V, Nag TC, Jain, S, Sreenivas V, Wadha S, 2013. Prenatal loud music and noise: differential impact on physiological arousal, hippocampal synaptogenesis and spatial behavior in one day-old chicks. PLoS One 8:e67347.