Behavioral syndromes across time and space in a long-lived turtle

Behavioral syndromes are correlated behaviors across different contexts and are critical for understanding processes in the ecology and evolution of animal personality. To aid in this endeavor, there is a need to study syndromes in wild animals from understudied species over long timescales. We investigated behavioral syndromes in wild ornate box turtles (Terrapene ornata) across four distinct populations over four different years. We measured three behavioral traits (boldness, activity, and exploration) in controlled trials using standardized 10-min assays on 174 different turtles 314 times. Overall, turtles demonstrated consistent correlations between behavioral traits, indicating conserved behavioral syndromes in this species. A behavioral syndrome between activity and exploration was detected in every population in every year except one in 2016, suggesting a strong conserved basis for these traits to covary. Correlations with boldness and other behavioral traits were also consistent but their magnitude varied. At least two populations did not exhibit relationships in two different years, one population’s syndrome strength changed from one year to the next, and another population exhibited a relationship in one year only. Boldness and activity were fully decoupled in one population, underscoring the significance of syndromes in coping with environmental variability for a long-lived ectothermic vertebrate. This is the first study to document behavioral syndromes along the boldness, activity, and exploration axes in a wild terrestrial turtle. Our results emphasize the need to preserve behavioral diversity while maintaining syndrome integrity alongside genetic and ecological diversity, which together will promote the conservation of ornate box turtles.

Methods
Please see the original protocols for collecting behavioral data described in Reed et al. (2023) as those data formed the basis of our study. Below are brief explanations of how this dataset was collected and processed.

Data collection:

We studied behavioral syndromes across four separate years (2016, 2020, 2021, and 2022) in four ornate box turtle (Terrapene ornata) populations from the Midwest. Behavior assays for boldness, activity, and exploration were conducted in all four populations following the same protocol in all years. Assays for each behavior were 10 minutes long and conducted in a fixed order with turtle order randomly assigned each day. We performed assays in the mornings (between 0700–1200 hr) over two consecutive days (starting the morning after the turtle was collected from the field). To start trials, turtles were placed in test arenas, at which point a timer was started, and then observers moved behind “blinds” to record data. Boldness was measured as the time for the turtle to emerge from the den in seconds. Activity was measured as the number of quadrant transitions around a circular track. Exploration was measured as the number of transitions between equal-sized quadrants with arched openings.

Data processing:

We used the average of two assays (day 1 and day 2) as the behavioral score for an individual turtle within a year. As factors, we included sex, population, year, and body size as curved carapace length in mm. We used all turtles for data analysis (174 turtles measured 314 times, which encompassed 95 turtles with measurements from at least 2 years), including turtles that did not emerge from the den during a boldness assay, which were scored as taking the maximum time possible (600 seconds for emergence). We also included turtles that exhibited zero quadrant transitions in either an activity or exploration assay. 

Original paper with a description of the behavioral data collection: 

Reed, B.M., K. Hobelman, A. Gauntt, M. Schwenka, A. Trautman, P. Wagner, S. Kim, C. Armstrong, S. Wagner, A. Weller, K. Brighton, S. Bloom, C. Nelson, F. Suboh, C. Kolthoff, S. Dukuly, R.J. Mercader, and D.F. Hughes. 2023. Spatiotemporal variation of behavior and repeatability in a long-lived turtle. Behavioral Ecology and Sociobiology 77: 88. 

https://doi.org/10.1007/s00265-023-03360-4