Like terrestrial animals, wild fish exhibit individual differences in daily activity patterns, known as chronotypes. However, monitoring free-living fish has posed challenges in studying chronotypes and their plasticity in response to the environment. To address this issue, we utilized high-throughput telemetry to measure daily activity in a large group of free-living pearly razorfish, Xyrichtys novacula, while also monitoring fine-scale environmental variables. Using hidden Markov models for behavioural segmentation, we quantified four circadian-related traits (awakening time, rest onset, activity duration relative to the daytime and rest midpoint relative to middle of the night) during two biological contexts (prespawning and spawning). We then used linear mixed-effects models to decompose the variation of these traits into individual, ecological (contextual environment) and population components. Our findings revealed the presence of chronotypes in both sexes, with greater between-individual variation in behaviour during spawning. Males exhibited longer activity duration due to an earlier awakening time than females, and temperature, waves and light significantly influenced daily activity behaviours. However, there was considerable individual variation in response to environmental changes, indicating the emergence of behavioural reaction norms (i.e. plasticity), with females showing greater plasticity in rest onset and relative rest midpoint. Our study also identified significant correlations among traits, suggesting that the activity duration continuum defines the pearly razorfish chronotype. Overall, our work represents the most comprehensive description of individual and ecological contextual variation in chronotypes within a wild marine fish population. It underscores the importance of environmental fluctuations in shaping the expression of internal clocks.

The research was carried out within the framework of the activities of the Spanish Government through the ‘Maria de Maeztu Centre of Excellence’ accreditation to IMEDEA (CSIC-UIB) (CEX2021-001198). The CLOCKS I+D+I project funded this work (grant no. PID2019-104940GA-I00) funded by MCIN/AEI/10.13039/501100011033 and the FSE invierte en tu futuro. The telemetry system was financed by the German Federal Ministry of Education and Research (Grant No. #033W024A). M.M.B. was supported by an FPI predoctoral fellowship from the Direcció General de Innovació i Recerca of the Balearic Islands Government (ref. FPI/2167/2018). E.A. was supported by a Margalida Comas (ref. PD/023/2018) and a Vicenç Mut (PD/041/2021) Postdoctoral Grants from the Government of the Balearic Islands and the European Social Fund. M.B.S. received funding from the European Union's Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No. WildFishGenes-891404.

With funding from the Spanish government through the ‘María de Maeztu Unit of Excelence’ accreditation (CEX2021-001198-M).

Peer reviewed