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.

What Birds belong in the "Clever Club"?

Nathan Emery's delightful and thoughtful book, Bird Brain An exploration of avian intelligence, should be read by all serious students of bird behavior.

Bird Brain brings together diverse research threads and makes them coherent. The book is notable for its economy of language, judicious selection of materials, and meticulous original illustrations that are tightly linked to the with the text.  It builds from Emery's previous suggestion that that crows, jays, and parrots should be thought of as Feathered Apes and should qualify as "members of the Clever Club." 

For much of the 20^th century, bird brains were undervalued. The prevailing scientific view of a bird's brain was superficial, wrong-headed, and based on faulty anatomy buttressed by an abiding unconscious preoccupation with a "tree of life" that leads upwards from microbes to man - thus reaffirming human exceptionalism.

Brains are the most complex and baffling of all organs, in birds and in humans. Since the first medieval human cadavers were exhumed for dissection, brain anatomists have been devising ponderous formal anatomical terminologies that came to be not only opaque but also misleading to non-specialists.

Only mammals have a well-developed 6-layered cerebral cortex and so that cortex came to be regarded as the hallmark of a top-quality brain.  Classical neuroanatomists reasoned that because birds lack such a cortex, then bird brains must be primitive feeble organs, capable of only simple automatic "instinctive" responses to stimuli.

Research in anatomy, molecular evolution, and behavior converged to refute those misconceptions of bird brains. The pivotal research was that of Harvey J Karten who traced the pathways from the ear to the higher audition centers of a pigeon's brain² in the mid-20^th century. Clumsy anatomical terminology was finally revolutionized in the early 21^st century^3,4,5.

High level mental capacities in birds may be localized in quite different anatomical locations than in mammals. Like mammals, bird brains have an executive center that organizes behavior over time.
Emery's drawing on the right depicts the executive centers (dark green) of a primate and of a crow as recently investigated by Onur Güntürkün at the University of Rhom^6,. The bird's executive center, the dark green NCL (nidopallium caudolaterale), is at the top rear in the crow's forebrain while the primate executive center, the  dark green PFC  (prefrontal cortex), lies behind the forehead above the eyes at the front of the forebrain.

The succeeding six chapters are the meat of the book.  Nathan Emery masterfully brings together research concerned with learning, memory, navigation, communication, self-awareness and tool using, to confirm the impressive cognitive capacities of birds.  These beautifully written and illustrated chapters critically showcase ongoing research of Emery himself (at the University of London), that of his wife Nicky Clayton (at the University of Cambridge), and incisive experiments of many other gifted biologists.

Nathan Emery made judicious choices as he picked his topics and examples, largely drawn from research on crows, parrots, jays, pigeons, and zebra finches.  However, the story that Emery tells is perforce incomplete because we have so much to learn about bird minds, bird cognition, and bird emotion, even in the few species where they have been studied. 

Birds comprise over 10,000 species in a lineage that has evolved for 300 million years in parallel to the lineage that gave rise to us mammals. The exquisite adaptations of birds for diverse life styles call for further research, and bird brains are excellent models for many universal mechanisms of brain function. 

We should all look again at the behaviors of the birds in our lives, to better understand birds and ourselves.

References:
1. Emery N, 2016. Bird Brain. An exploration of avian intelligence. Princeton University Press 
2. Karten, HJ, 1969. The organizaotin of the avian telencephalon and some speculations on the phylogeny of the amniote telencephalon. Ann  N Y Acad Sci 167:164-179.
3. Reiner A, Perkel DJ, (25 other authors), Jarvis ED, 2004.  Revised nomenclature for the avial telencephalon and some related brainstem nuclei. J Comp Neurol  473:377-414.
4. Jarvis ED, Güntürkün O, (25 other authors) Reiner A, Butler AB, 2005. Avian brains and a new understanding of vertebrate brain evolution. Nature Neurosci 6:151-159.
5. this blog earlier post  
6. Güntürkün O, 2005. The avian 'prefrontal cortex' and cognition,  Curr Opin Neurobiol 15:686-693.