Parental habituation to human disturbance over time reduces fear of humans in coyote offspring

Abstract

A fundamental tenet of maternal effects assumes that maternal variance over time should have discordant consequences for offspring traits across litters. Yet, seldom are parents observed across multiple reproductive bouts, with few studies considering anthropogenic disturbances as an ecological driver of maternal effects. We observed captive coyote (Canis latrans) pairs over two successive litters to determine whether among‐litter differences in behavior (i.e., risk‐taking) and hormones (i.e., cortisol and testosterone) corresponded with parental plasticity in habituation. Thus, we explicitly test the hypothesis that accumulating experiences of anthropogenic disturbance reduces parental fear across reproductive bouts, which should have disparate phenotypic consequences for first‐ and second‐litter offspring. To quantify risk‐taking behavior, we used foraging assays from 5–15 weeks of age with a human observer present as a proxy for human disturbance. At 5, 10, and 15 weeks of age, we collected shaved hair to quantify pup hormone levels. We then used a quantitative genetic approach to estimate heritability, repeatability, and between‐trait correlations. We found that parents were riskier (i.e., foraged more frequently) with their second versus first litters, supporting our prediction that parents become increasingly habituated over time. Second‐litter pups were also less risk‐averse than their first‐litter siblings. Heritability for all traits did not differ from zero (0.001–0.018); however, we found moderate support for repeatability in all observed traits (r = 0.085–0.421). Lastly, we found evidence of positive phenotypic and cohort correlations among pup traits, implying that cohort identity (i.e., common environment) contributes to the development of phenotypic syndromes in coyote pups. Our results suggest that parental habituation may be an ecological cue for offspring to reduce their fear response, thus emphasizing the role of parental plasticity in shaping their pups’ behavioral and hormonal responses toward humans.

Fear and stressing in predator–prey ecology: considering the twin stressors of predators and people on mammals

“…Bolder individuals are most likely to exploit novel opportunities and have reduced stress responses to human activity (Atwell et al, 2012). Animals that routinely encounter human activity, typically provide parental care, and are capable of reproducing multiple times across their life span may produce offspring that are acclimated to human activity and accordingly show lower fear/stress responses (Schell et al, 2018). Habituation of groups of animals to human activity is being increasingly observed, often as a result of bold individuals spending significant amounts of time around human-disturbed areas and displaying reduced fear responses (Stillfried et al, 2017).…”

Changes in the social behavior of urban animals: more aggression or tolerance?

“…For urban birds, the impact of light and noise pollution on the behavior has also been shown (Moiron et al 2015;Swaddle et al 2015;Weaver et al 2019). Various indicators were used to study these phenomena: from measurements of home ranges, risk-taking behavior, success in solving problems, escape response, diurnal activity, or aggression levels to more sophisticated indicators such as noise-dependent changes in vocalization, stress hormone levels, or genetic markers (e.g., Bonier 2012;Francis et al 2015;Meillere et al 2015;Moiron et al 2015;Vincze et al 2016;Santangelo et al 2018;Schell et al 2018;Łopucki et al 2019;Solaro and Sarasola 2019).…”

Maternal human habituation enhances sons’ risk of human-caused mortality in a large carnivore, brown bears

“…To our knowledge, this report is the first to indicate that the level of maternal human habituation, as well as offspring birthplace, age, and sex, determines the likelihood of human-caused mortality of the offspring at early stages of life, not only in bears, but also in large carnivores. Whether bears born to highly habituated mothers also become highly habituated is unclear; however, offspring adoption of parental habituation to humans has been reported in coyotes (Canis latrans) 45 , another carnivorous species. Social learning passed from mothers to their offspring would be a primary determinant of the level of human habituation.…”