Hypoxia increases the behavioural activity of schooling herring: a response to physiological stress or respiratory distress?

Atlantic herring, Clupea harengus, increase their swimming speed during low O(2) (hypoxia) and it has been hypothesised that the behavioural response is modulated by the degree of respiratory distress (i.e. a rise in anaerobic metabolism and severe physiological stress). To test directly whether a deviation in physiological homeostasis is associated with any change in behavioural activity, we exposed C. harengus in a school to a progressive stepwise decline in water oxygen pressure (P(O2) = 20.4, 15.2, 12.7, 10.6, 8.5, 6.4 and 4.2 kPa) and measured fish swimming speed and valid indicators of primary and secondary stress (i.e. blood cortisol, lactate, glucose and osmolality). Herring in hypoxia increased their swimming speed by 11-39% but only when P(O2) was < 8.5 kPa and in an unsteady (i.e. declining) state. In parallel with the shift in behaviour, plasma cortisol also exhibited an increase with P(O2) <= 8.5 kPa, plasma osmolality was subject to a transient rise at 8.5 kPa and plasma glucose was generally reduced at P(O2) <= 12.7 kPa. However, without any rise in anaerobically derived lactate levels, there was no evidence of respiratory distress at any set P(O2). We show that a shift in physiological homeostasis is indeed linked with an increase in the swimming speed of herring but the physiological response reflects a hypoxia-induced shift in metabolic fuel-use rather than respiratory distress per se. The significance of this behavioural-physiological reaction is discussed in terms of behavioural-energetic trade-offs, schooling dynamics and the hypoxia tolerance of herring.