Testing the predictions of coping styles theory in threespined sticklebacks

Abstract

Coping styles theory provides a framework for understanding individual variation in how animals respond to environmental change, and predicts how individual differences in stress responsiveness and behavior might relate to cognitive differences. According to coping styles theory, proactive individuals are bolder, less reactive to stressors, and more routinized than their reactive counterparts. A key tenet of coping styles theory is that variation in coping styles is maintained by tradeoffs with behavioral flexibility: proactive individuals excel in stable environments while more flexible, reactive individuals perform better in variable environments. Here, we assess evidence for coping styles within a natural population of threespined sticklebacks (Gasterosteus aculeatus). We developed a criterion-based learning paradigm to evaluate individual variation in initial and reversal learning. We observed strong individual differences in boldness, cortisol production, and learning performance. Consistent with coping styles, fish that released more cortisol were more timid in response to a predator attack and slower to learn a color discrimination task. However, there was no evidence that reactive individuals performed better when the environment changed (when the rewarded color was reversed). The failure to detect trade-offs between behavioral routinization and flexibility prompts other explanations for the maintenance of differing coping styles.

Keywords: Animal personality; Coping styles; Cortisol; Individual differences; Learning; Threespined stickleback.

Fig. 1

Experimental set up. a) Top-down view of tank set up for boldness assay. Kiddie pool was divided into 9 sections and marked A–I. Starting shelter was placed in the middle of section A. Black symbols in each section represent stones that were placed for investigation and additional shelter. Top-down view of the tank set up for training trials. Fish were acclimated to environment by repeatedly being placed in the starting shelter and then allowed to make a choice. The same set up was also used for actual training trials. Striped regions show the choice regions. Once a fish entered either of these regions, its choice was noted. b) Photo of sculpin model used for boldness assay. c) Top-down view of the tank set up for training trials. Fish were acclimated to environment by repeatedly being placed in the starting shelter and then allowed to make a choice. The same set up was also used for actual training trials. Striped regions show the choice regions. Once a fish entered either of these regions, its choice was noted.

Fig. 2

Cortisol repeated measures. a) Average cortisol release rate across the five sampling periods. Cortisol release rate was significantly lower 270 min after the start of isolation compared to 30 min (n = 10). b) Individual differences in average cortisol release rate across the two sampling weeks. Each line represents an individual fish (n = 10).

Fig. 3

Boldness measures. a) Repeatability of boldness (total sections entered after predator attack) across four days. Each line represents an individual fish (n = 10), with the same symbols for individuals as in Fig. 2b. One individual (Fish 10) died after day 3. b) Difference in activity before and after predator attack. Fish moved less after the attack suggesting that predator model was perceived as a threat by the fish. The values on the y-axis represent the number of times each fish moved into a different section of the pool over the time observed. Grey lines indicate the average behavioral change in response to the predator attack for each individual fish, with the same symbols for individuals as in Fig. 2b.

Fig. 4

Individual learning curves during the a) initial learning, and b) reversal learning discrimination phases. Lines represent the performance of individuals across sessions, with the same symbols for individuals as in Fig. 2b. Criterion was reached when the proportion of correct choices was greater than or equal to 0.8 (marked by horizontal grey line) on two consecutive sessions. Note the poor performance during the first and second sessions of the reversal learning phase, suggesting that fish initially relied on the previously-learned association.

Fig. 5

Scatterplots showing results consistent with coping styles theory. Each data point represents a different individual, coded by sex (open circles = females, closed circles = males) a) Bolder individuals (i.e., fish that entered more sections after the predator attack) had lower average cortisol release rates across two weeks. b) Bolder individuals reached criterion in the initial color discrimination task in fewer sessions. c) Individual fish with higher average cortisol release rates took more sessions to reach criterion in the initial color discrimination task.