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Learning Before Birth

Reed warbler does not realise that the cuckoo chick is not its own.

This reed warbler does not realise that the cuckoo chick it is feeding is not its own.

By Sonia Kleindorfer and Jeremy Robertson

Superb fairy-wrens sing to their chicks before they hatch, teaching them a begging call that identifies them before cuckoo chicks can predate the nest.

Our capacity to wonder, and to communicate that wonder, sets us apart from many animals. But when does communication about the external world begin?

The BirdLab at Flinders University recently discovered that communication occurs before birth, at least in some birds, and that it is crucial for survival. We found that female superb fairy-wrens teach their unhatched embryos a unique acoustic element that is the basis of their begging call.

Our discovery came about by chance. Because nest predation is the major cause of avian mortality, we monitored the inside of nests 24 hours per day with a microphone and video camera in order to identify nest predators. We successfully observed some nest predation, but more startling was our discovery that the mother wrens sing a previously unknown vocalisation – we called it the incubation call – to their eggs for a few days before they hatch.

This struck us as odd, because a female calling in her nest several times an hour for four or five days could attract predators to her extremely vulnerable eggs or very young nestlings. This suggests there must be a very large benefit for females that take the risk of producing these calls.

After they hatched, the wren siblings in each nest produced the same begging call, and each nest had a begging call that was significantly different from the begging call given in neighbouring nests. The begging call of each family was unique because it was based on a unique element in the newly discovered incubation call of each mother.

Was this match of the unique element in each mother’s incubation call and the begging calls of her offspring due to inheritance (genetic programming), or did the female teach them the unique element by calling to the embryos?

To separate the genetic effects from the effect of rearing environment, we swapped the clutches of eggs between nests. We recorded the incubation calls of the biological and foster mothers, and the begging calls of the nestlings after they hatched.

This experiment separates the two possibilities: if the characteristic begging calls were due to genetics then the nestling begging calls would match the incubation call of their biological mother. If they were due to learning they would match the incubation call of their foster mother.

To our great delight we confirmed that females were teaching the embryos. The call similarity between the foster females and the nestlings was much higher than between the nestlings and their genetic mother.

Why do females teach the nestlings a particular begging call note? Like many birds, superb fairy-wrens are parasitised by cuckoos, which lay their eggs in the wren nest. Subsequently the cuckoo nestling ejects the host eggs and nestlings, and deceives the host parents into rearing it.

The cuckoo hatches earlier than the host egg, so the cuckoo hatchling can evict the host eggs or young hatchlings before they can resist eviction. The parent wrens then invest 2 weeks of their lives to feed the cuckoo nestling that has killed their family.

This is hugely costly to the hosts because they fail to rear any of their own young and waste time and energy rearing an unrelated parasite. There are thus huge selective pressures to detect and abandon nests that have been parasitised by cuckoos so that the host parents can attempt to produce another brood of their own offspring.

Intriguingly, superb fairy-wrens are one of very few species in the world that can identify cuckoo nestlings, which they then abandon to starve. It was thought that they detected the cuckoos using acoustic cues because the shining bronze-cuckoo that always fails to parasitise the wrens has a very dissimilar begging call.

Conversely, the begging call of the Horsefield’s bronze-cuckoo resembles the begging call of the superb fairy-wren. There thus appears to be an arms race between the cuckoos and their wren hosts, with the cuckoo mimicking the begging calls of the wrens, while it is advantageous for the wrens to keep their begging calls distinct so they can detect cuckoo nestlings that fail to achieve a sufficiently good match.

Our recently discovered nest-specific begging calls that have a learned and unique element from the mother’s incubation calls seems to provide a further refinement in this arms race to give the wrens an edge. Perhaps the mothers are teaching their offspring a unique password just before they hatch so that she can distinguish them from a cuckoo that may be in her nest.

We tested this hypothesis with playback experiments in which a loudspeaker placed under the nest could broadcast a begging call from that nest (the control), a neighbouring nest or a cuckoo nestling. Thus we tested whether parent wrens can detect a strange wren nestling versus a cuckoo nestling.

We monitored the response with a video camera in the nest and watched the parents outside the nest from a concealed vantage point. At the very least they should scrutinise the nestlings with greater vigilance and perhaps abandon the nest for having been parasitised by a cuckoo nestling with a mismatched begging call.

The results were clear-cut. As expected, there was no effect on parental feeding when we played a begging call recorded at the nest; the stimulus just added to the collective begging of the nestlings and matched their calls. When the stimulus was a wren begging call from another nest, the parents did not feed their nestlings and flew around the nest, giving alarm calls. The parents’ response was exactly the same when a cuckoo begging call was played.

Thus it seems the unique aspect of the wren begging calls at each nest plays a key role in detecting intruders, and thus the females teaching their offspring the password element just before they hatch may have a critical role in the arms race with cuckoos.

How did the male wrens know when the begging calls mismatched the password element in the mother’s incubation call? Males are not present when females produce the incubation call, so how can they learn the password?

To test whether males also learned the begging call password, we placed audio recorders throughout the territory and recorded female and male communication between the parents. To our amazement, we found that female wrens, when away from the nest, approached their mate and produced a solicitation call to induce the male to feed her. The solicitation call contained the password! After hearing the solicitation call, the male would feed the female, and also be informed about the secret begging call.

Our observations and experiments tell us that the function of the begging call password is to expose intruder cuckoo nestlings. Our discovery and experiments have uncovered adult abandonment of offspring that did not learn as embryos.

Sonia Kleindorfer and Jeremy Robertson are senior lecturers in the School of Biological Sciences at Flinders University. This article is adapted from Issues magazine (