Cardiorespiratory physiology of farmed Atlantic salmon in a warming climate and implications for growth and swimming performance

<p dir="ltr">The Atlantic salmon (<i>Salmo salar</i> L.) is an anadromous species widely cultured for human consumption around the globe and currently represents the main aquaculture species farmed in Tasmania, Australia. Tasmanian waters are a climate change hotspot where summer temperatures can exceed 19 °C for extended periods, which is above the optimal temperature for salmon growth in seawater (~15 °C). Thermal tolerance is partially limited by the capacity of the cardiovascular system to meet increased oxygen demand at elevated temperatures. Although the salmon heart can acclimate to challenging environmental conditions through physiological plasticity, this capacity might be hindered in farmed salmonids as they appear more prone to develop cardiac abnormalities compared to their wild counterparts. Further, impaired cardiovascular capacity coupled with cardiac abnormalities may negatively affect growth as well as important physiological traits such as swimming performance, resulting in premature mortality and production losses. In the face of rapid climate change, it is both commercially and scientifically relevant to better understand the extent of salmon cardiac phenotypic plasticity in response to suboptimal temperatures, and the underlying mechanisms through which cardiac plasticity is achieved. This thesis investigates the effect of suboptimal elevated temperatures on the development of cardiac morphological abnormalities with the aim of inferring their overall effect on cardiac performance, along with potential implications for growth and swimming performance in post-smolt and grow-out Tasmanian Atlantic salmon.<br>Across two experiments, I examined the effect of suboptimal elevated temperatures on morphological remodelling of the heart as well as the molecular mechanisms that may underlie such physiological responses in adult Atlantic salmon. Further, I investigated how different feeding strategies may affect fat deposition on the surface of the heart (epicardial fat) and inferred its potential link with cardiac function and performance. The first experiment investigated salmon cardiac morphology, specifically focusing on ventricular roundness (measured as height/width ratio) and the angle between the bulbus arteriosus and the ventricle. Results revealed no significant differences between adult salmon (~1.5 kg) held for 133 days at the optimal temperature for Atlantic salmon (15 °C) and those held at a suboptimal elevated temperature (19 °C). This observation held true even when the salmon were fed two commercial feeds with different dietary energy levels. However, epicardial fat was significantly higher in fish reared at the elevated temperature and fed a high-energy diet relative to a low-energy diet, while the same effect was not apparent at the optimal temperature.<br>Given no absolute differences in cardiac morphology between temperatures in the first experiment, a second experiment aimed to examine whether cardiac morphology changed over time in Atlantic salmon exposed to a simulated summer-autumn temperature profile during grow out. Temperatures during this period were characterised by an incremental increase (1 °C per day) from 15 to 19.5 °C, 84 days at 19.5 °C (elevated temperature), and finally, a decremental decrease (1.5 °C per day) from 19.5 to 15 °C, and then 34 days at 15 °C (optimal temperature). Although the angle between the bulbus arteriosus and the ventricle increased significantly during the elevated temperature period relative to initial conditions, ventricular roundness was not significantly different between the three temperature periods. Similarly, there were no significant changes in gene expression of biological markers of cardiac remodelling.<br>Thermal stress imposed by suboptimal elevated temperatures in association with sustained aerobic exercise may compromise a fish’s cardiorespiratory performance, growth, and welfare, thereby limiting their ability to cope with environmental and anthropogenic stressors. In this context, segregating fish based on their swimming ability has been proposed as a tool for the selection of individuals with inherently superior cardiac performance and overall robustness, which may increase resilience to extreme weather conditions typical of offshore farming. In the final experiment of this PhD project (consisting of two sub-experiments), I investigated how cardiac shape is associated with growth, aerobic metabolism, and swimming capacity in post-smolt Atlantic salmon (~350 g) reared under suboptimal elevated temperature and either low- or high-intensity aerobic training. To achieve this, post-smolt salmon were reared for 90 days at optimal and elevated temperatures (15 and 20 °C, respectively) while continuously exercising at low and high intensities (water velocity 0.18 m.s^-1 and 0.45 m.s^-1 , respectively). Subsequently, in the first sub-experiment, I used swim-tunnel respirometry to test the effect of the two training intensities on aerobic swimming performance of individual fish reared at 20 °C. Further, I measured a range of cardiac parameters (ventricular roundness, bulbus misalignment, epicardial fat area, relative ventricular mass; RVM) in individual fish following respirometry. In the second sub-experiment, I segregated post-smolt salmon from the same population based on their swimming performance into either good swimmers or poor swimmers to determine if phenotypic variation in swimming performance could be linked to improved growth rate, blood oxygen carrying capacity (haematocrit and haemoglobin concentration), and cardiac morphology under the two temperatures and training intensities. Overall, the results from the first sub-experiment showed that aerobic scope [the difference between the fish’s standard metabolic rate (SMR) and maximum rate of aerobic metabolism (MMR)], as well as the maximum swimming speed of fish reared at 20 °C, was not affected by training regime. Cardiac morphological parameters were largely consistent between the two training regimes, with the notable exception of RVM. This parameter showed a significant increase in fish swimming at high intensity compared to those at low intensity. In the second sub-experiment, there were no observed differences in growth either between the two groups of swimmers or between the two training regimes. However, fish raised at the optimal temperature displayed a significantly higher growth rate compared to those at the elevated temperature. In terms of cardiac anatomy, poor swimmers trained at low intensity displayed a more rounded ventricle under both optimal and elevated temperatures compared to those trained at high intensity. Conversely, this effect was not observed for good swimmers. In conclusion, the results from this thesis highlight the capacity of the heart of farmed Atlantic salmon to maintain certain aspects of its structure and function when exposed to temperature-related stress over prolonged periods. While some parameters showed no change across experiments, others exhibited variations, underscoring the nuanced response of salmon to suboptimal elevated temperatures. Although cardiac malformations are frequently reported in salmon aquaculture and have been linked to sudden mortality of seemingly healthy salmon, our findings suggest that rearing Tasmanian Atlantic salmon at suboptimal elevated temperature under experimental conditions does not induce maladaptive remodelling of cardiac structure. Moreover, this work showed the outstanding swimming and aerobic capacity of Tasmanian Atlantic salmon, thereby providing promising data for salmon farming in harsher environments typical of offshore locations. However, given the imminent challenges posed by climate change, transient heat waves, and the myriad of stressors salmon typically face in farming conditions, further research is crucial. Specifically, delving deeper into the role of cardiac performance in fish health and welfare will be essential to prevent production losses in the future.</p>