Zebra finches are highly-social and learn foraging skills from their parents. However, if exposed to stress after hatching, young birds will ignore their parents and look to unrelated adult birds for help and learning instead.

Researchers say that spikes in stress in hatchlings may cue young birds that their parents are doing something wrong, triggering them to switch their social learning strategy and disregard parental approaches in favor of acquiring skills exclusively from other birds in the flock.

Stress cues and subsequent behavioral changes allow the juvenile birds to bypass a "potentially maladaptive source of information" - a result of low-quality parental interest, or food scarcity at birth - in order to avoid a "bad start in life," say researchers. Stress creates changes in patterns of social interactions by impeding population-wide processes, such as efficient migration and the establishment of bird culture.

The new study is published today in the journal Current Biology.

"These results support the theory developmental stress may be used as an informative cue about an individual's environment. It may enable juveniles to avoid becoming trapped in a negative feedback loop provided by a bad start in life. By programming them to adopt alternative, and potentially more adaptive behaviors, they can change their developmental trajectories."

Neeltje Boogert PhD, Department of Zoology, University of Cambridge, Cambridge, UK and the School of Psychology and Neuroscience, University of St. Andrews, St. Andrews, UK — authored the study with colleagues from the universities of Oxford and St Andrews, UK.

The research team took 13 broods of zebra finch hatchlings and in each brood fed half of the chicks the stress hormone corticosterone dissolved in peanut oil, and the other half with just plain peanut oil (their control siblings). The chicks were fed corticosterone each day from the age of 12 days, for 16 more days.

Once the chicks reached nutritional independence, they were released with their families into free-flying aviaries. Researchers then tracked their social foraging networks. Unique radio tags or PIT tags (Passive Integrated Transponder), about the size of a grain of rice, had been inserted in each bird. When a bird visited a feeder, the bird's PIT tag was scanned allowing researchers to know exactly who was foraging where, when and with whom.

"If developmentally stressed birds occupy more central network positions and follow many others around, this might make them especially efficient spreaders of disease, as stressed individuals are also likely to have weakened immune systems."

Neeltje Boogert PhD

Using the feeder visit data, researchers were able to define finch social foraging networks over the course of 40 days. They found that the juveniles fed the stress hormone were less likely to spend time with their parents, spending more time with unrelated birds, and were far less choosy about which birds they foraged with. Whereas the control group stuck more closely to their parents and foraged more consistently with the same flock mates.

To test whether these stress-hormone induced differences in social network positions affected who learned from whom, Boogert devised a food puzzle for the birds, and recorded exactly when each bird started solving it.

In the new test, birds had to flip the lids off the top of a grid of holes to reach the spinach food reward underneath. All other feeders were removed from the aviaries, as researchers filmed a series of nine one-hour trials over three days, monitoring and scoring how each bird learned to get to the spinach.

They found while the control group of juveniles also learned from some unrelated adults, they principally copied their parents to learn how to get the spinach. In sharp contrast, the developmentally-stressed chicks exclusively copied unrelated adults - not one looked to a parent to figure out the key to the spinach puzzle.

In fact, stressed juvenile birds actually solved the task sooner than their control siblings — despite not using parents as role models. Boogert believes this may be because they relied more on trial-and-error learning, or because they copied a large number of unrelated adults rather than just one of their two parents and simply got the key idea sooner.

"The next step is to explore the implications of our results for important population-level processes, such as the spread of avian pox or flu."

Abstract Highlights
•Juvenile zebra finches learn foraging skills from their parents
•Stress hormone exposure triggers juveniles to learn from unrelated adults instead
•Stress may be a cue juveniles use to inform their behavioral strategies
•Switching social learning strategy may alter developmental trajectories adaptively

Summary
Stress during early life can cause disease and cognitive impairment in humans and non-humans alike [ 1 ]. However, stress and other environmental factors can also program developmental pathways [ 2, 3 ]. We investigate whether differential exposure to developmental stress can drive divergent social learning strategies [ 4, 5 ] between siblings. In many species, juveniles acquire essential foraging skills by copying others: they can copy peers (horizontal social learning), learn from their parents (vertical social learning), or learn from other adults (oblique social learning) [ 6 ]. However, whether juveniles’ learning strategies are condition dependent largely remains a mystery. We found that juvenile zebra finches living in flocks socially learned novel foraging skills exclusively from adults. By experimentally manipulating developmental stress, we further show that social learning targets are phenotypically plastic. While control juveniles learned foraging skills from their parents, their siblings, exposed as nestlings to experimentally elevated stress hormone levels, learned exclusively from unrelated adults. Thus, early-life conditions triggered individuals to switch strategies from vertical to oblique social learning. This switch could arise from stress-induced differences in developmental rate, cognitive and physical state, or the use of stress as an environmental cue. Acquisition of alternative social learning strategies may impact juveniles’ fit to their environment and ultimately change their developmental trajectories.

This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

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