Conservationists often raise the young of endangered species in captivity before releasing them into suitable habitats as adults. The benefits are obvious: survival to adulthood is typically high, as captive animals are safe from predators and food scarcity. Unfortunately, a lack of exposure to enemies in early life may become a drawback later, if the released individuals have never learned to recognize and avoid their predators.
One way to fix this is 'antipredator training', where young animals are confronted with fake or real predators and taught to associate these with an unpleasant stimulus. However, this method is labor-intensive and depends on the realism of the training and the ability and most sensitive period for learning of the captive species. But now, researchers may have found a more efficient alternative: train the mothers instead.
"Here we show, for the first time in an endangered mammal, that predator training of pregnant mothers can influence how their offspring respond to predators later in life," said Dr Debra Shier, the Brown endowed associate director of recovery ecology at , San Diego Zoo Wildlife Alliance in Escondido, California, and the senior author of the study in Frontiers in Ecology and Evolution .
"Female offspring of predator-trained mothers were more vigilant during predator encounters, suggesting that maternal experiences may shape offspring behavior in ways that could be useful for conservation breeding and reintroduction programs."
Snake in the grass
Shier and her coauthor Dr Catherine T.Y. Nguyen here studied the effects of antipredator training on pregnant females of the Pacific pocket mouse (Perognathus longimembris pacificus), classified as critically endangered on the IUCN's Red List and protected under the US Endangered Species Act.
They conducted a randomized controlled experiment with two arms on 22 pregnant females in the second half of gestation. Each trial was filmed and lasted 20 minutes. Half of the females were assigned to the predator-exposed treatment, in which they were placed in a testing arena with food. After acclimatization, a live kingsnake (a native predator of small mammals) was introduced behind a wire mesh across the arena. Pocket mice were sprayed with water whenever they approached the snake. The mice received scores for behavior, location, and orientation relative to the snake. The remaining pregnant females were assigned to the control, where the snake was replaced with a rope of similar length. Control females were never sprayed.
Once pups had been born (87 in total) and reached 30 days of age, the scientists tested their behavior towards a snake following the same protocol. A subset of 44 offspring were then released into suitable habitat at within coastal southern California, while their post-release survival was assessed through live trapping towards the end of the summer active season.
No animals were harmed during the study, which had been approved by the Institutional Animal Care and Use Committee of the San Diego Zoo Wildlife Alliance and was conducted in agreement with California and federal law.
Wee, sleekit, cow'rin, tim'rous beastie
The results showed that in the snake's presence, daughters of predator-trained mothers displayed more vigilance behaviors like scanning, freezing, and rearing up to monitor their surroundings and assess potential threats. However, no such difference was found between sons of predator-trained mothers and sons of control mothers.
The authors concluded that giving anti-snake training to pregnant females makes their daughters, but apparently not their sons, more cautious around snakes.
Does this mean that at least females whose mothers had been trained survive better in the wild? The authors did not find any boost on survival after release. But they caution against concluding too quickly that no beneficial effects exist, given the small sample size and that all mice underwent exposure to snakes before release.
And how might the learned caution towards snakes have been transmitted from trained mothers to their female offspring?
"One possibility is prenatal programming, where stress hormones associated with predator training during pregnancy influenced offspring development before birth. Another is that the mothers behaved differently after the pups were born, which could likewise shape the latter's behavior. It is also possible that pups detected lingering odor cues from the antipredator training in their mother," hypothesized Shier.
"We don't yet know why female offspring responded differently than males, but sex-specific responses to stress and predator cues have been observed in other species. Maternal predator training may have amplified those innate differences."
