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Movement modeling and patterns of within- and among-individual behavioral variation across time scales in neonate garter snakes (Thamnophis elegans)

Abstract

Animal movement modeling and animal personality frameworks are both useful approaches to identify patterns of behavioral variation. Yet these approaches are seldom applied jointly, especially in the context of a controlled laboratory experiment. In this study, we combine these approaches to identify patterns in the behavior of neonate snakes at different time scales (within several minutes of a trial and across the days of the experiment). Specifically, we utilize Bayesian hierarchical hidden Markov models on fine-scale movement data and Bayesian mixed linear models on additional behavioral data (average movement speed, tongue-flick rate, latency to emerge, and area explored) measured repeatedly in captive-born western terrestrial garter snakes (Thamnophis elegans). This novel approach identified distinct behavioral states that describe movement patterns and predictable patterns of transitions in behavioral states at different time scales. Snakes exhibited consistent among-individual variation for all traits, and behaviors were correlated across contexts. Patterns of behavioral changes over time demonstrate responsiveness consistent with habituation, a basic form of learning, but snakes did not learn to associate a novel object with a simulated attack. Our unique approach provides a useful case study in how the joint application of statistical methodologies often relegated to different fields can be leveraged to describe personality axes and to characterize shifts in behavior at short (minutes) and long (across days) time scales in an experimental design context.

Significance statement

Using a combination of traditional statistical approaches and novel movement modeling, we identified patterns in the behavior of baby snakes at different time scales (within several minutes of a trial and across the days of the experiment). Snakes were consistent in their behaviors and exhibited individual differences in these behaviors. Further, behaviors were correlated across contexts: snakes that were more active in an open field test were also more likely to emerge from a hide and explore. Over time, snakes decreased their responsiveness to repeated stimuli, which suggests a basic form of learning. However, we found no evidence that snakes could learn to associate a novel object with a simulated attack within the timeframe of our experiment.

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Data availability

Data from this study are available on Figshare (https://figshare.com/s/e69f4326bcc80fda8cb4).

Code availability

Code used for analyses (R and Stan) are available as supplemental materials associated with this manuscript.

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Acknowledgements

We thank M. Barazowski, C. Corwin, C. Hinsley, and A. Wendt for assistance with behavior assays and animal care and A. Sparkman, S. Zylstra, K. Martin, and T. Rickman for fieldwork support. G. Burghardt, P. Dixon, and R. Langrock provided important statistical advice. The manuscript was improved by constructive comments from R. Joo and an anonymous reviewer. We are also grateful to the participants and organizers of the Statistical Issues in Ecology and Evolutionary Biology seminar at ISU, spring 2015.

Funding

This work was supported by funding from the US National Science Foundation (IOS-0922528), the Iowa Science Foundation (15–11), and the American Society of Ichthyologists and Herpetologists Gaige Fund. EJG received additional support from the ISU Office of Biotechnology.

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Authors and Affiliations

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Contributions

Experiment was designed and protocols developed by EJG, CDK, and AMB. Data were analyzed by EJG and VL-B with support from GD and HZ. Manuscript was drafted by EJG and VL-B with input on revisions from all authors.

Corresponding author

Correspondence to Eric J. Gangloff.

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Ethics approval

Fieldwork was conducted with the permission of the California Department of Fish and Game (#SC-11973). The Institutional Animal Care and Use Committee (IACUC) at Iowa State University approved all procedures (protocol # 1–12-7285-J), and we adhered to the Guidelines for use of Live Amphibians and Reptiles in Field and Laboratory Research (Beaupre et al. 2004). At the conclusion of the experiment, mothers were released at the point of capture, and offspring were maintained in the lab colony. We followed established animal care protocols to carefully monitor the health of these animals and to minimize stress before, during, and after the procedures described here.

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Not applicable.

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Not applicable.

Conflict of interest

The authors declare no competing interests.

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Communicated by S. Joy Downes

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Gangloff, E.J., Leos-Barajas, V., Demuth, G. et al. Movement modeling and patterns of within- and among-individual behavioral variation across time scales in neonate garter snakes (Thamnophis elegans). Behav Ecol Sociobiol 75, 162 (2021). https://doi.org/10.1007/s00265-021-03099-w

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  • DOI: https://doi.org/10.1007/s00265-021-03099-w

Keywords

  • Behavioral syndrome
  • Boldness
  • Habituation
  • Hierarchical hidden Markov models
  • Movement models
  • Personality