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

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

Envir_GrpCharact_Stress_upload_Dryad

The file contains the response variable (monthly mean fecal glucocorticoid metabolite levels N=1,094), fixed effects (ecological and social factors), and random effects (groups and gorillas ID) entered in the GLMM as described in the manuscript

Data from: Social and ecological factors alter stress physiology of Virunga mountain gorillas (Gorilla beringei beringei)

Living in a rapidly changing environment can alter stress physiology at the population level, with negative impacts on health, reproductive rates, and mortality that may ultimately result in species decline. Small, isolated animal populations where genetic diversity is low are at particular risks, such as endangered Virunga mountain gorillas (Gorilla beringei beringei). Along with climate change‐associated environmental shifts that are affecting the entire population, subpopulations of the Virunga gorillas have recently experienced extreme changes in their social environment. As the growing population moves closer to the forest's carrying capacity, the gorillas are coping with rising population density, increased frequencies of interactions between social units, and changing habitat use (e.g., more overlapping home ranges and routine ranging at higher elevations). Using noninvasive monitoring of fecal glucocorticoid metabolites (FGM) on 115 habituated Virunga gorillas, we investigated how social and ecological variation are related to baseline FGM levels, to better understand the adaptive capacity of mountain gorillas and monitor potential physiological indicators of population decline risks. Generalized linear mixed models revealed elevated mean monthly baseline FGM levels in months with higher rainfall and higher mean maximum and minimum temperature, suggesting that Virunga gorillas might be sensitive to predicted warming and rainfall trends involving longer, warmer dry seasons and more concentrated and extreme rainfall occurrences. Exclusive use of smaller home range areas was linked to elevated baseline FGM levels, which may reflect reduced feeding efficiency and increased travel efforts to actively avoid neighboring groups. The potential for additive effects of stress‐inducing factors could have short‐ and long‐term impacts on the reproduction, health, and ultimately survival of the Virunga gorilla population. The ongoing effects of environmental changes and population dynamics must be closely monitored and used to develop effective long‐term conservation strategies that can help address these risk factors

Coyote Population Pedigree

This datafile contains pedigree information for all individual pups and parents included in the study. The 'pedantics' package was used on these data to determine pedigree specifications and summary statistics for the pedigree used in all Bayesian animal models. These data can be found in the Supporting Information Table S1

Coyote Pup Hormones_pt.2

This aggregated file contains information on pup cortisol, testosterone, and risk-taking behavior to perform the multivariate analyses used to determine correlation estimates among traits (risk-taking with cortisol; cortisol with testosterone; and risk-taking with testosterone). Data for each individual were binned according to the period of hair sample collection. Hence, hair collected at 10 weeks of age were paired with the aggregate number of foraging "successes" (i.e. "1") over the 5-10 week developmental period. To use a "multinomial2" distribution, the column "FR.total" was included with "FR.success", which creates a proportional matrix of how often the individual ate in front of an observer. All other columns are identical to the files "Coyote Pup Hormones_pt.2" and "Coyote Risk-taking Assays

R Code_Coyote Parental Fear

Complete and annotated R script used for all analyses. The data files denoted in this Dryad repository are named and linked to all of the code in this file. Thus, Bayesian animal models performed, model selection analyses, correlation estimates, highest posterior density intervals (HPDI), and model assessment lines of code are all contained in this file

Coyote Risk-Taking Assays

This CSV file contains all foraging (i.e. risk-taking) assay data, for both pups and parents, over the 5-15 week study period. Each row represents a single observation for each individual in order to assess repeated measures in pups/parents. The "animal", "dam", and "sire" columns are synonymous to those found in the 'Coyote Pedigree' file attached; this was done as a requirement by the 'MCMCglmm' package, which needs all three columns to structure data around the pedigree. The column titled "Lit.ID" denotes the litter identity of each pup, the variable used to observe common environment effects using MCMCglmm. The "ID" column is identical to the "animal" column, but is necessary in order to partition additive genetic effects from permanent environment effects (see Wilson et al. 2010 - An Ecologist's Guide to the Animal Model). The column "Age" denotes the age of the pup/litter when the observation occurred, the "life.stage" partitions pup observations from adult observations, and the "Dev.Period" column partitions the weaning and post-weaning periods (i.e. 5-9 week observations and 10-14 week observations, which can be traced back to the "Age" column). The "risk.success" column represents whether an individual foraged or not during an observation (i.e. "0" for no, and "1" for yes), whereas the "risk.total" column is always equal to "1", denoting the total number of observations. This column is only important insofar as the way in which you choose to analyze the data in the MCMCglmm package. If using the distribution family argument "multinomial2", then the "risk.total" column is used as the second variable in that dependent variable form. Further - "Lit.size" denotes litter size of the pup/adult, "Year" (either 1st or 2nd) denotes the year of observation and the parity of the parent, "Sex" is self-explanatory, and "Trmt" indicates the PARENTAL odor treatment group, which occurred BEFORE the pups were born (see Schell et al. 2016 - Olfactory attractants and parity affect prenatal androgens and territoriality of coyote breeding pairs)

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

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