Use of accelerometer technology for individual tracking of activity patterns, metabolic rates and welfare in farmed gilthead sea bream (Sparus aurata) facing a wide range of stressors

Abstract

The biosensor technology has the potential to revolutionize the aquaculture industry, but the selection of tagging method, operational mode (stand-alone vs. wireless systems) and telemetry technology ultimately depends on living species, life stage and research question. In particular, AEFishBIT is a small and stand-alone device composed of a tri-axial accelerometer, a microprocessor, a battery, and a RFID tag that was designed to be externally attached to the operculum. This unique location serves to provide simultaneous measurements of activity patterns (signals of x- and y-axes) and respiratory frequency (z-axis signal) processed by on-board algorithms. The validity of measurements was initially proved in exercised fish in a swim tunnel respirometer, and its use as a reliable tool for the individual monitoring of whole-organism traits in free-swimming gilthead sea bream was tested then in fish facing a wide range of biotic and abiotic stressors. The impact of the tagging method, based on the use of monel piercing fish tags with a flexible heat shrink polyethylene ring, was also evaluated and no signs of growth impairment, operculum damage or gill lamellae haemorrhage were found 10 days post-tagging. The autonomy of the device was 6 hours of continuous recording with re-programmable lag times and recording schedules of 2 min windows at regular intervals along the experimental period (2-8 days). Such procedure underlined a negative linear correlation between fasting weight loss and operculum breaths, becoming respiratory frequency a reliable indicator of basal metabolic rates. Biosensing signals also highlighted the more continuous physical activity and increased respiratory rates of young fish when comparisons were made between one- and three-year old fish. Also, AEFishBIT measurements evidenced a generalized increase of respiratory frequency during severe hypoxia (2-3 ppm), but the individuals classified as proactive fish also shared an increased physical activity for supporting escape reactions in a milieu with low oxygen availability. Likewise, we also observed an overall increase of physical activity with the decrease of tank space availability, which can contribute to establish stricter criteria of welfare in farmed fish. Finally, the reduction of respiratory frequency was a consistent diagnostic marker of the progression of parasitic enteritis in experimentally infected fish with the myxozoan Enteromyxum leei. Altogether, this work constitutes the proof of concept of the use of biosensor technology as a reliable tool for individual fish phenotyping of whole-organism traits in farmed fish, contributing to improve animal welfare and productivity of aquaculture industry.