Animal behaviour

A social call

An indicator of animal intelligence is thought to be the ability to judge relationships between members of the same species. This talent, previously seen only in primates, seems to be evident in a bird.

In mixed company: Vignal et al.3 find that male zebra finches (with orange cheek patches and chestnut flanks) respond to their mate's call in a manner that depends on the social context. Credit: E. JANES/NHPA

Zebra finches are small, colonial songbirds native to Australia, and they have been favourite subjects of biologists for years1. Most studies have focused on the birds' vocal-communication behaviour, and many insights have emerged from such research. For example, female zebra finches can recognize their mate, with whom they form lasting pair bonds, by his ‘distance call’, one of the most frequent vocalizations of these finches2. But the early studies found no reciprocal recognition — male zebra finches did not recognize their mate through female distance calls. The reason for this was unclear, although it was speculated that, as the females' calls have a simpler acoustic structure than those of the males, the calls contained fewer individually recognizable features.

One overlooked factor was the context in which these recognition tests were conducted. The birds, normally members of large flocks in the wild or large groups in captivity, had been tested while alone. On page 448 of this issue, Vignal et al.3 suggest not only that female zebra finch distance calls are individualized, but that social isolation in the previous tests was the primary cause of the male's apparent recognition failure. They go a step further, showing that, remarkably, the males respond to their mate's calls according to the social situation. This latter finding suggests for the first time that a non-primate may be able to assess the social relationships between other animals of its own species, an ability thought to be a mark of intelligence.

To determine whether the females' distance calls had the potential for individual recognition, Vignal et al.3 analysed the acoustic structure of calls from seven female zebra finches. Several features were measured to characterize each female's call. By quantifying the variability of each acoustic feature in each bird and comparing these with the variability found for the group, Vignal et al. concluded that certain features were sufficiently individualized to allow recognition. Further, when these features were analysed in more detail, the authors found that they could identify individual females with 100% accuracy. Clearly, males should be able to identify their mate's calls. Why, then, was this not seen before? And what might facilitate this recognition process in male zebra finches? The answer seems to lie in the birds' brains.

Two neurobiological studies4,5 of brain activation during singing in zebra finches found that the areas of the brain responsible for song production and for perception are differentially activated according to the social context in which the bird is placed. Both in vivo electrophysiological recordings and assessment of early gene activity indicated that different brain areas are activated depending on whether the males are singing alone or with a female. As all previous studies of mate recognition by male zebra finches were conducted when the bird was alone, could it be that differences in social context modify recognition behaviour in an analogous way to the modification of brain-activation patterns?

To address this question directly, Vignal et al.3 played back either the mate's call or a familiar female's call to male zebra finches in three different ‘social’ conditions: with two unmated males, with a mated pair or with an unmated pair. The results were striking. When male zebra finches were with either unmated males or an unmated pair, they showed no greater response to their mate's call than to the call of a familiar female. That is, males called back at about equal rates in response to both their mate's calls and those of the familiar female. But when males were exposed to calls in the presence of a mated pair, the differences were marked: males called back almost twice as often in response to their mate's calls as to the familiar female's calls.

These results are intriguing on several levels, and will undoubtedly provide fodder for future research. First, Vignal et al. show that even a seemingly simple call can contain enough information to be identified individually. Equally interesting is how this comes about in female zebra finches, which until now had been thought to be unable to learn vocalizations like males of the species. Further, how do social context and the male's recognition ability interact? Do males recognize their mates in all social situations but express this ability only in certain ones? Or does the social situation itself activate the brain areas required for recognition, facilitating the recognition process?

Perhaps the most important implication of this study is that we primates are not alone in our ability to judge social context. It seems that birds are far more aware of such niceties than we have previously given them credit for.

References

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Sturdy, C. A social call. Nature 430, 414 (2004). https://doi.org/10.1038/430414a

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