Seasonal changes in weather, food availability and mice body condition
The weather was hot and dry during summer (temperature: 24.42 ± 0.36 °C; total rainfall: 0.60 mm) and temperatures were lower and rainfall was higher during the winter months (temperature: 13.47 ± 0.45 °C; total rainfall: 39.60 mm; LM: N = 138, F = 368.4, P < 0.001; F = 4.31, P = 0.039, respectively). Food availability for the striped mice increased within the study period from summer (2.35 ± 0.11 food plants/plot) to winter (3.27 ± 0.24 food plants/plot; LM: Nsummer plots = 48, Nwinter plots = 48, F = 12.12, P < 0.001).
Body mass and length were greater in winter than summer (body mass: summer: 41.33 ± 1.01 g; winter: 47.17 ± 1.29 g; LMM: N = 107, χ21 = 13.44, P < 0.001; Length: summer: 106.21 ± 0.95 mm; winter: 113.91 ± 1.21 mm; LMM: N = 107, χ21 = 30.41, P < 0.0001). Males were heavier than females in both seasons (LMM: N = 107, χ21 = 38.38, P < 0.0001; summer males: 44.46 ± 1.47 g; summer females: 38.09 ± 1.13 g, t-test: Nmales = 31, Nfemales = 27, t96 = − 3.33, P = 0.006; winter males: 52.20 ± 1.37 g; winter females: 40.29 ± 1.47 g; LMM: N = 44, χ21 = 31.54, t-test: Nmales = 30, Nfemales = 19, t96 = − 5.56, P < 0.001). Males were longer than females in both seasons (LMM: N = 107, χ21 = 34.55, P < 0.0001; summer: males: 109.21 ± 1.30 mm; females: 102.00 ± 0.99 mm, t-test: Nmales = 31, Nfemales = 27, t88 = − 3.62, P = 0.003; winter: males: 118.12 ± 1.42 mm; females: 108.37 ± 1.43 mm, t-test: Nmales = 30, Nfemales = 19, t96 = -− 4.71, P = 0.0001).
Seasonal changes in learning and reversal learning
Initial task acquisition
All mice (N = 107, Table 1) opened the door for 3 consecutive trials. Some mice did not succeed to open the door at their first attempt and hence needed 4 trials to open doors for 3 consecutive trials (summer: 0/58; winter: 4/49). There was no significant influence of season (GLMM, N = 107, χ21 = 0.01, P = 0.985) and sex (GLMM, N = 107, χ21 = 0.00, P = 0.999). There was no influence of the season and sex on latencies to open the doors during the 3 consecutive successful trials (LMM, N = 107, 1st trial: season: χ21 = 1.40, P = 0.235; sex: χ21 = 0.43, P = 0.509; 2nd trial: season: χ21 = 2.09, P = 0.148; sex: χ21 = 0.21, P = 0.649; 3rd trial: season: χ21 = 3.48, P = 0.062; sex: χ21 = 0.28, P = 0.597; Supplementary Information: Table 1). However, longer mice showed a greater latency to succeed during their first trial (LMM, N = 107, χ21 = 5.38, P = 0.020).
Learning task
Overall, we tested 87 of the 107 mice in the learning task since 20 mice were not re-trapped within 6 days after the initial task acquisition phase (Table 1). The learning task was achieved by all subjects within 13.48 ± 0.33 (range: 12–23) trials.
There was no significant influence of season and intrinsic (age, body mass, length) characteristics on the trials to criterion (TTC) and the overall accuracy during the learning task (Table 2). However, there was a significant interaction between season and sex for the mean latency to succeed (LMM, N = 87, χ21 = 6.67, P = 0.009). Males tested in winter showed longer latencies compared to females tested in summer (t-test : Nfemales summer = 24, Nmales winter = 22, t45 = − 3.32, P = 0.009; Nfemales summer = 24, Nfemales winter = 17, t40 = 0.63, P = 0.921; Nfemales summer = 24, Nmales summer = 24, t47 = − 1.23, P = 0.609; Nfemales winter = 17, Nmales summer = 24, t40 = − 1.10, P = 0.689; Nfemales winter = 17, Nmales winter = 22, t40 = − 1.84, P = 0.269; Nmales summer = 24, Nmales winter = 22, t45 = − 1.14, P = 0.667; Fig. 1a).
Mean latency ± SEM (in seconds) for all trials needed to reach the learning criterion by season and sex. Males tested in winter showed longer latencies both during the (a) the learning task (Nfemales = 41; Nmales = 46) and (b) the reversal learning task (Nfemales = 38; Nmales = 40). Post hoc t test with Tukey correction, *P ≤ 0.05.
Reversal learning
We tested 78 of the 87 mice in the reversal learning task since 9 mice were not re-trapped within 6 days after the learning task (Table 1). Reversal was attained by all tested subjects within 14.37 ± 0.28 (range: 12–24) trials. There was no significant influence of the season and intrinsic characteristics on the accuracy during the reversal learning task (Table 3). However, there was a significant interaction between season and sex on the trials to criterion (LMM, N = 78, χ21 = 4.02, P = 0.045). Females tested in summer tended to need fewer trials to reach the learning criterion compared to females tested in winter (t-test: Nfemales summer = 22, Nfemales winter = 16, t37 = − 2.57, P = 0.058; Nfemales summer = 22, Nmales summer = 23, t44 = − 1.15, P = 0.660; Nfemales summer = 22, Nmales winter = 17, t38 = − 0.44, P = 0.971; Nfemales winter = 16, Nmales summer = 23, t38 = 1.26, P = 0.589; Nfemales winter = 16, Nmales winter = 17, t32 = 1.54, P = 0.419; Nmales summer = 23, Nmales winter = 17, t39 = 0.49, P = 0.959). There was an influence of season on the mean latency to succeed (LMM, N = 78, χ21 = 6.67, P = 0.009). Mice tested in winter showed longer latencies compared to those tested in summer (t-test: Nsummer = 45, Nwinter = 33, t39 = − 3.27, P = 0.011; Fig. 1b).
Learning curve
Learning curves representing accuracy computed for the 12 first successive trials showed a significant effect of trial number (GLMM, N = 87, χ21 = 44.59, P < 0.001), which is indicative of learning since the accuracy increased with trial number from the 3rd trial (t-test: Trial 1 versus Trial 3 to 12, P < 0.05 for all, Fig. 2a). In addition, there was a significant interaction between season and sex on the response accuracy (GLMM, N = 87, χ21 = 4.44, P = 0.035; Fig. 2a). Males tested in summer showed slower improvement in accuracy in learning compared to males tested in winter (t-test: Nmales summer = 24, Nmales winter = 22, t45 = − 2.97, P = 0.015; Nmales summer = 24, Nfemales summer = 24, t47 = 1.89, P = 0.231; Nmales summer = 24, Nfemales winter = 17, t40 = 0.17, P = 0.998; Nfemales summer = 24, Nfemales winter = 17, t40 = − 0.12, P = 0.999; Nfemales summer = 24, Nmales winter = 22, t45 = − 1.13, P = 0.670; Nfemales winter = 17, Nmales winter = 22, t40 = 0.08, P = 0.999; Fig. 2a). For the reversal learning task, there was a significant effect of trial number (GLMM, N = 78, χ21 = 150.47, P < 0.001): accuracy increased with trials number from the 3rd trial onwards (t-test: Trial 1 versus Trial 3 to 12, P < 0.05 for all, Fig. 2b). There was a significant interaction between season and sex on the response accuracy (GLMM, N = 78, χ21 = 6.97, P = 0.008; Fig. 2b). Females tested in summer showed faster improvement in accuracy in reversal learning compared to females tested in winter (t-test: Nfemales summer = 22, N females winter = 16, t36 = 2.81, P = 0.025; Nfemales summer = 22, Nmales summer = 23, t44 = 1.86, P = 0.246; Nfemales summer = 22, Nmales winter = 17, t38 = 0.49, P = 0.961; Nfemales winter = 16, N males summer = 23, t38 = − 1.11, P = 0.685; Nfemales winter = 16, Nmales winter = 17, t32 = − 2.15, P = 0.138; Nmales summer = 23, Nmales winter = 17, t39 = − 1.16, P = 0.648; Fig. 2b).
Learning curves in (a) the learning (Nfemales = 41; Nmales = 46) and (b) the reversal learning tasks (Nfemales = 38; Nmales = 40), for the 12 first successive trials. The left panels show males and right panel females. Mice tested in summer are represented with black dots and full black lines and mice tested in winter are represented with grey triangles and gray dashed lines. Post hoc t test with Tukey correction, *P ≤ 0.05.
Speed-accuracy trade-off
For the learning task, there was a significant influence of the latency (LMM: N = 87, χ21 = 8.57, P = 0.004) and the interaction between latency and season (LMM: N = 87, χ21 = 7.16, P = 0.009), but no influence of sex (LMM: N = 87, χ21 = 1.08, P = 0.301) on accuracy: in winter, mice of both sexes which required more time to solve the task were less accurate (Spearman rank correlation, summer: rs = − 0.23, P = 0.111; winter: rs = − 0.61, P < 0.001; Fig. 3a). For the reversal learning task, there was no significant influence of the latency (LMM: N = 78, χ21 = 0.11, P = 0.741), the interaction between latency and season (LMM: N = 78, χ21 = 0.99, P = 0.321) and sex (LMM: N = 78, χ21 = 0.17, P = 0.683) on accuracy (Fig. 3b).
Influence of the season on speed accuracy trade-off measured by the relationship between mean latency (seconds) calculated from all trials during (a) the learning (N = 87) task and (b) the reversal learning tasks (N = 78); and accuracy measured as the number of correct responses divided by the total number of responses (Spearman rank correlation, ***P < 0.001).
Source: Ecology - nature.com
