These birds learn their mother’s calls whilst still in their eggs | @GrrlScientist

A recently-published study reveals that nestlings of Australia’s Red-backed Fairy-wrens learn their mother’s calls before they hatch. The parents rely upon these calls to identify their chicks and invest more effort into raising nestlings whose calls are most similar to their own.

by GrrlScientist for Forbes | @GrrlScientist

Female Red-backed Fairy-wren (Malurus melanocephalus), Samsonvale, SE Queensland, Australia. (Credit: Aviceda/CC BY-SA 3.0.)

Fairy-wrens Are Very Good Listeners

A few years ago, scientists discovered that female superb fairy-wrens, Malurus cyaneus, teach their chicks a special “vocal password” before they even hatch (ref & ref). This strategy is just one of several that apparently evolved during the so-called “arms race” between fairy-wrens and their brood parasites. Teaching their chicks a special vocal password allows fairy-wren parents and their nest helpers to identify and to preferentially feed their own chicks whilst mostly ignoring chicks of other species that are snuck in their nests.

The sneaky species, Horsfield’s bronze-cuckoo, Chrysococcyx (Chalcites) basalis, and brush cuckoos, Cacomantis variolosus, are brood parasites that lay an egg or two into the fairy-wrens’ nests, in the hope that their chicks will deceive the fairy-wren parents into preferentially feeding and caring for them. Since even newly-hatched superb fairy-wren chicks can produce their mother’s vocal password, whilst cuckoo chicks cannot, experienced fairy-wren parents are not fooled by these interlopers.

Adult Horsfield’s bronze-cuckoo (Chrysococcyx basalis), Capertee Valley, NSW, Australia. (Credit: Aviceda/CC BY-SA 3.0.)

But superb fairy-wrens aren’t the only fairy-wren species that are parasitised by cuckoos. Knowing this, the lead author of the original studies, behavioral ecologist Diane Colombelli-Négrel, now a fully-fledged postdoctoral researcher at Flinders University in Australia, wondered whether this particular behavioral strategy is unique to superb fairy-wrens, or if other fairy-wren species also teach their offspring a special vocal password whilst their chicks are still embryos?

“After we discovered embryonic learning in superb fairy-wrens, we started to question how widespread this phenomena was”, said Dr Colombelli-Négrel in email.

“The red-backed fairy-wrens, being close relatives of the superb fairy-wrens, were the ideal choice to start answering this question”, said Dr Colombelli-Négrel.

Female Red-backed Fairy-wrens Sing to Their Eggs

Dr Colombelli-Négrel’s initial discovery that female superb fairy-wrens sing, or call, to their eggs was a very lucky accident (ref).

“Because fairywrens have high predation rates, we originally placed microphones under Superb Fairywren nests to record alarm calls against predators, twenty-four seven”, said Dr Colombelli-Négrel about her previous research.

“As a result, we discovered embryonic learning in Superb Fairywrens.”

Brisbane field site where one of the study populations of red-backed fairy-wrens live. (Credit: Diane Colombelli-Negrel/The Auk.)

To establish whether female red-backed fairy-wrens, Malurus melanocephalus, also teach their chicks a vocal password, Dr Colombelli-Négrel and her team replicated their earlier superb fairy-wrens study. They placed microphones under red-backed fairy-wren nests and recorded all vocalisations for two continuous hours each morning between days 10 and 14 of incubation. They also recorded nestling begging calls at 36 of the 67 nests for two continuous hours per nest between days 3 and 7 of the nestling phase. Eleven of those 36 nests were also recorded daily from hatching.

Spectrogram analysis of the red-backed fairy-wrens’ vocalisations revealed that two types of song elements (elements A and B in Figure 1) are contained in female red-backed fairy-wrens’ nest calls. Further, the analysis found that one of those song elements, element B (which is also referred to as the “signature element”), was faithfully replicated by newly hatched nestlings (Figure 1):

FIGURE 1. Spectrograms from four nests (two from the Brisbane site and two from the Cairns sites) showing some examples of the two element types described in this study: element A and element B; element B is also known as the signature element. (Credit: Diane Colombelli-Négrel et al.; doi:10.1642/AUK-15–162.1)

After the team established that female fairy-wrens sang whilst incubating their eggs, and that their nestlings dependably produced the signature element in their mother’s nest song, they then wanted to know if the chicks were learning their mother’s special signature element whilst still embryos? This meant they also had to determine whether, or if, the females sang to their chicks after they hatched. To answer these questions, the researchers monitored all nests (67 in total) and found that 62% of the females continued to call after hatching, stopping only five or six days after hatching (Figure 2):

FIGURE 2. Percentage of nests at which incubation and post-hatching calls were detected after the onset of hatching: data are presented separately for Brisbane (in grey) and Cairns (in black). (Credit: Diane Colombelli-Négrel et al.; doi:10.1642/AUK-15–162.1)

“The one thing that surprised me with the red-backed fairy-wrens is the fact that female red-backed fairy-wrens, unlike superb fairy-wrens, had a different temporal pattern for their calling behaviour: they started at day 5 of incubation and continued until 5 days after hatching”, said Dr Colombelli-Négrel in email. She noted that this behavior contrasted with superb fairy-wrens, who only called during the last few days of incubation, and stopped after the chicks hatched.

Nestlings Imitate Song Elements in Their Mother’s Calls

To determine whether the chicks were specifically imitating their mother’s calls instead of those produced by, say, another female nesting nearby, Dr Colombelli-Négrel and her team recorded a total of 619 incubation and post-hatching calls from 27 females at the Brisbane site and 1,040 incubation and post-hatching calls from 40 females at the Cairns sites. They also recorded the female and her nestlings at 10 nests (267 begging events recorded in total) at the Brisbane site and at 26 nests (968 begging events) at the Cairns sites.

Spectrogram analysis of the nestlings’ begging calls revealed they were significantly different between nests. Additionally, spectrogram analysis also showed that each female’s signature element was significantly different from other signature elements produced by any other female (Figure 3):

FIGURE 3. Average SPCC values (mean ± SE) for (1) within vs. between female element B comparison, (2) within vs. between chick calls comparison, and (3) females vs. their own and other young element B comparison. The data are presented for (a) Brisbane (n = 27) and (b) Cairns (n = 40). (Credit: Diane Colombelli-Négrel et al.; doi:10.1642/AUK-15–162.1)

Not only were the nestlings’ begging calls most similar to the incubation calls produced by their mother, and this similarity was strongly related to the number of incubation and post-hatching calls produced per hour during incubation, yet this similarity was not related to the calls produced by the chicks’ mother later, during the nestling period (Figure 4):

FIGURE 4. A positive correlation between incubation call rate and call similarity (regression weighted by site: β = 0.34, p = 0.05, n = 33). (Credit: Diane Colombelli-Négrel et al.; doi:10.1642/AUK-15–162.1)

Chicks Whose Begging Calls Were Most Similar To Their Mother’s Calls Received More Food

To test the importance of the nestlings’ begging call similarity to that of the mother’s signature element, Dr Colombelli-Négrel and her team conducted playback experiments where they broadcast nestling begging calls that they had recorded at five other nests on their study sites. These broadcasted recordings featured the begging calls made by hungry nestlings that were the same age as those in the study nest.

The team found that red-backed fairy-wren parents were more likely to feed nestlings associated with broadcasted recordings that sounded most like the mother’s own song element B (Figure 5):

FIGURE 5. Percentage of nest visits that resulted in food delivery to nestlings (% successful feeds) in relation to call element similarity between the attending female’s element B and the experimental nestling begging calls: we found that nestlings were fed significantly more when nestling element similarity was higher. (Credit: Diane Colombelli-Négrel et al.; doi:10.1642/AUK-15–162.1)

Female Fairy-wren Call Rate Was Not Affected By Cuckoo Abundance

But why did the fairy-wren chicks have to produce begging calls that were very similar to their mother’s signature element? Dr Colombelli-Négrel’s original work indicated that it was important for the parent birds to distinguish their nestlings from those of brood parasitic cuckoos. So Dr Colombelli-Négrel and her colleagues tested that hypothesis, and were surprised to find that the rate at which red-backed fairy-wren mothers called to their eggs did not increase significantly when more cuckoos were present in the habitat (Figure 6):

FIGURE 6. Nestling begging call element similarity in relation to cuckoo prevalence, defined as either lower (number of nests with evidence of parasitism ,1.5%) or higher (number of nests with evidence of parasitism .3%). We found that element similarity between mother and young was higher when parasitism prevalence was higher (F1, 35 1⁄4 4.82, p 1⁄4 0.03) at the Brisbane site, but not at the Cairns sites. Bars depict mean +/- SE. (Credit: Diane Colombelli-Négrel et al.; doi:10.1642/AUK-15–162.1)

This was not what they expected. Which raises the question: what is the evolutionary reason for the parents’ bias towards nestlings that best replicate their mother’s calls? In the light of these new findings, Dr Colombelli-Négrel and her colleagues speculate that the similarity of nestlings’ calls to the mother’s calls may indicate which nestlings are the healthiest and the best learners, so the parents can then invest more resources into those that are most likely to thrive — distinguishing their own chicks from cuckoo chicks might be an added bonus.

Cuckoo hatchling in a red-backed fairy-wren nest. (Credit: Diane Colombelli-Negrel/The Auk.)

Vocal Learning Occurs Earlier In Birds Than We Ever Knew

“One of the main takeaway messages from this study is that ‘through the egg’ learning may be a common phenomenon in birds, and something worthy of more research attention,” said William Feeney, a Postdoctoral Research Fellow in the School of Biological Sciences at the University of Queensland.

“So far, it has only been demonstrated in two closely related Australian fairy-wren species, so similar studies in different genera is required to determine how wide spread this phenomenon is, as well as its purpose,” said Dr Feeney in email.

Dr Feeney, who is an expert on the interactions between cuckoos and their host birds, then pointed out: “The authors suggest that it may be related to identifying brood parasitic chicks (ie. cuckoos) so that they can accordingly discriminate against them by abandoning the parasitised nest (cuckoos evict the host’s own chicks, making brood parasitism particularly costly to the host). This is an interesting idea that requires further investigation. While this current study did not produce significant results in its support, this may be expected as red-backed fairy-wrens experience lower levels of parasitism compared to the superb fairy-wren. It would be interesting to conduct further research to see if non-host species also exhibit through the egg learning,” said Dr Feeney.

Might the mother’s incubation calls endanger her eggs and nest?

“In contrast to previous work on the superb fairy-wren, they found no evidence that the mother’s ‘incubation’ call rate affected rates of nest predation,” said Dr Feeney.

“This may simply be because red-backed fairy-wrens generally experience lower levels of nest predation compared to superb fairy-wrens, making it harder to detect an effect (I have noticed that red-backed fairy-wrens are much more secretive than superbs in the field),” said Dr Feeney. “It may also suggest that there are other reasons that may underpin this ability (such as indicating “good learners” to parents).”

This research indicates that early vocal learning may be more commonplace amongst songbirds than thought.

“[T]his study is important as it provides evidence for a second species that has this ability and raises questions regarding why it may have evolved in the first place,” said Dr Feeney.

“Fairywrens have become a new model system in which to test new dimensions in the ontogeny of parent-offspring communication in vertebrates,” agreed the study’s co-author, animal behaviorist Mark Hauber, a professor of comparative psychology at Hunter College.

This research makes me wonder whether early vocal learning is typical for all fairy-wren [Maluridae] species? Dr Colombelli-Négrel and her collaborators are already working on answering this question; collecting more data on superb, red-backed, splendid, variegated, and red-winged fairy-wrens.

“We also would like to extend our work to species other than Maluridae to investigate if females in general call to their eggs and their potential benefits”, said Dr Colombelli-Négrel.

Adult male Red-backed Fairy-wren (Malurus melanocephalus). (Credit: J Welkin/The Auk.)

Source:

Diane Colombelli-Négrel, Michael S. Webster, Jenelle L. Dowling, Mark E. Hauber, and Sonia Kleindorfer (2016). Vocal imitation of mother’s calls by begging Red-backed Fairywren nestlings increases parental provisioning, The Auk: Ornithological Advances 133 273–285 | doi:10.1642/AUK-15–162.1

Also cited:

Colombelli-Négrel D., Hauber M., Robertson J., Sulloway F., Hoi H., Griggio M. & Kleindorfer S. (2012). Embryonic Learning of Vocal Passwords in Superb Fairy-Wrens Reveals Intruder Cuckoo Nestlings, Current Biology, 22(22):2155–2160 | doi:10.1016/j.cub.2012.09.025

Diane Colombelli-Négrel, Mark E. Hauber, Sonia Kleindorfer (2014). Prenatal learning in an Australian songbird: habituation and individual discrimination in superb fairy-wren embryos, Proceedings of the Royal Society of London B, 281(1797):20141154 | doi:10.1098/rspb.2014.1154

W. E. Feeney, I. Medina, M. Somveille, R. Heinsohn, M. L. Hall, R. A. Mulder, J. A. Stein, R. M. Kilner, and N. E. Langmore (2013). Brood Parasitism and the Evolution of Cooperative Breeding in Birds, Science, 342(6165):1506–1508 | doi:10.1126/science.1240039 [$]

Read more about red-backed fairy-wrens: Birds Sing Duets To Reduce Cheating

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Originally published at Forbes on 27 April 2016.

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