In reference to the Great Depression, Franklin Delano Roosevelt is famously quoted as stating during his 1933 inaugural speech “the only thing we have to fear is fear itself.” Roosevelt was no biologist, but his words could equally apply to a different type of depression – the decline of animal populations that can be caused by fear.

Roosevelt’s inauguration in 1933. Credit: Architect of the Capitol.

Ecologists have long known that predators can depress prey populations by killing substantial numbers of their prey. But only in the past two decades or so have they realized that predators can, simply by their presence, cause prey populations to go into decline. There are many different ways this can happen, but, in general, a predation threat sensed by a prey organism can interfere with its feeding behavior, causing it to grow more slowly, or to starve to death. As one example, elk populations declined after wolves were introduced to Yellowstone National Park. There are many factors associated with this decline, but one factor is fear of predators causes elk to spend more time scanning and less time foraging. Also, elk tend to stay away from wolf hotspots, which are often places with good elk forage.

Liana Zanette recognized that ecologists had not considered whether predator presence can cause bird or mammal parents to reduce the amount of provisioning they provide to dependent offspring, thereby reducing offspring growth and survival, and slowing down population growth. For many years, she and her colleagues have studied the Song Sparrow, Melospiza melodia, on several small Gulf Islands in British Columbia, Canada. In an early study, she showed that playbacks of predator calls reduced parental provisioning by 26%, resulting in a 40% reduction in the estimated number of nestlings that fledged (left the nest). But, as she points out, Song Sparrow parents provision their offspring for many days after fledging; she wondered whether continued perception of a predation threat during this later time period further decreased offspring survival and ultimately population growth.

The Song Sparrow, Melospiza melodia. Credit: Free Software Foundation.

Zanette’s student, Blair Dudeck, did much of the fieldwork for this study. The researchers captured nestlings six days after hatching , weighed and banded them, and fit them with tiny radio collars. They then recaptured and weighed the nestlings within a few hours of fledging (at about 12 days post-hatching) to assess nestling growth rates.

Banded sparrow nestling with radio antenna trailing from below its wing. Credit: Marek C. Allen.

Three days after the birds fledged, Dudeck radio-tracked them, and surrounded them with three speakers approximately 8 meters from where they perched. For one hour, each youngster listened to recordings of calls made by predators such as ravens or hawks, followed, after a brief rest period, by one hour of calls made by non-predators such as geese or woodpeckers (or vice-versa). During the playbacks, Dudeck observed the birds to record how often the parents visited and fed their offspring, and whether offspring behavior changed in association with predator calls. This included recording all of the offspring begging calls.

Blair Dudeck simultaneously uses a tracking device to locate Song Sparrows and a recorder mounted to his head to record their begging calls. Credit: Marek C. Allen.

Fear had a major impact on parental behavior. Parents reduced food provisioning vists by 37% when predator calls were played in comparison to when non-predator calls were played. They also fed offspring fewer times per visit, which resulted in 44% fewer meals in association with predator calls.

Mean number of parental provisioning visits (in one hour) in relation to whether predator (red) or non-predator (blue) calls were played. Error bars are 1 SE.

Hearing predator calls had no effect on offspring behavior – they continued to beg for food at a high rate, and did not attempt to hide.

Some parents were much more scared than others – in fact, some parents were not scared at all. The researchers measured parental fearfulness by subtracting the number of provisioning visits by parents during predator calls from the number of visits during non-predator calls. A more positive number indicated a more fearful parent (a negative number represents a parent who fed more in the presence of predator calls). The researchers discovered that more fearful parents tended to have offspring that were in poorer condition at day 6 and at fledging.

Offspring weight on day 6 (open circles) and at fledging (solid circles) in relation to parental fearfulness.  Higher positive numbers on x-axis indicate increasingly fearful parents.

Importantly, more fearful parents tended to have offspring that died at an earlier age. Based on this finding, the researchers created a statistical model that compared survival of offspring that heard predator playbacks throughout late-development with survival of offspring that heard non-predator playbacks during the same time period. They estimated a 24% reduction in survival. Combined with their previous study on playbacks during early development, the researchers estimate that hearing predator playbacks throughout early and late development would reduce offspring survival by an amazing 53%.

This “fear itself” phenomenon can extend to other trophic levels in a food web. For example recent research by Zanette and a different group of researchers showed that playbacks of large carnivore vocalizations dramatically reduced foraging by raccoons on their major prey, red rock crabs. When these carnivore playbacks were continued for a month, red rock crab populations increased sharply. This increase in crab population size was followed by a decline of the crab’s major competitor – the staghorn sculpin, and the crab’s favorite food, a Littorina periwinkle. Thus “fear itself” can cascade through the food web, affecting multiple trophic levels in important ways that ecologists are now beginning to understand.

note: the paper that describes this research is from the journal Ecology. The reference is Dudeck, B. P., Clinchy, M., Allen, M. C. and Zanette, L. Y. (2018), Fear affects parental care, which predicts juvenile survival and exacerbates the total cost of fear on demography. Ecology, 99: 127–135. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.