Warming affects routine swimming activity and novel odour molecular response in larval zebrafish

Abstract

Temperature is a primary factor affecting the survival, development, and physiology of aquatic ectothermic animals and global warming of water bodies may therefore impact several biological levels of aquatic life. Understanding the effects of near-future predicted temperature changes on the behaviour and the underlying molecular mechanisms of aquatic animals is of particular importance, since behaviour mediates key interactions and, in turn, population dynamics. In this study, we investigate the effects of elevated developmental temperature on locomotor behaviour and olfactory learning in the zebrafish, Danio rerio. We exposed zebrafish from cleavage embryonic stage to either current day control (28°C) or predicted future elevated temperature (30°C) for seven days. Overall, warming reduced the total routine swimming distance and caused the upregulation of a small number of genes involved in metabolism and neuron development, suggesting accelerated development at elevated temperature. When fish were exposed to two different olfactory cues, namely catfish cue, a non-alarming but novel odour, and injured conspecifics alarm cue expected to cause a fear reaction, warming differently affected larvae response to the two cues. In particular, a large transcriptional reprogramming was observed at elevated temperature in response to novel odour exposure, with upregulation of cell signalling, neuron development and neuron functioning genes. As this response was coupled with downregulation of genes involved in protein translation and ATP metabolism, it indicates that novel odour recognition in future-predicted thermal conditions will require energetic trade-offs between expensive baseline processes and responsive functions. To also evaluate their learning abilities at both temperatures, 7 days post fertilization (dpf) zebrafish were conditioned with a mixture of injured conspecifics alarm cue and non-alarming catfish cue. Regardless of temperature, no behavioural (freezing) nor gene expression changes were detected, reinforcing our previous findings that warming mainly affects zebrafish molecular response to novel odours. Overall, our results show that future thermal conditions will likely impact developing stages, causing energy trade-offs following olfactory detection of novel substances in the environment.