Ventilation rates and activity levels of juvenile jumbo squids under metabolic suppression in the oxygen minimum zones

Abstract

Summary The Humboldt (jumbo) squid, Dosidicus gigas, is a part-time resident of the permanent oxygen minimum zone (OMZ) in the Eastern Tropical Pacific and, thereby, it encounters oxygen levels below its critical oxygen partial pressure. To better understand the ventilatory mechanisms that accompany the process of metabolic suppression in these top oceanic predators, we exposed juvenile D. gigas to the oxygen levels found in the OMZ (1% O2, 1kPa, 10ºC) and measured metabolic rates, activity cycling patterns, swimming mode, escape-jet (burst) frequency, mantle contraction frequency and strength, stroke volume and oxygen extraction efficiency. In normoxia, the metabolic rates varied between 14 to 29 µmol O2 g (ww)-1 h-1, depending on the level of activity. The mantle contraction frequency and strength was linearly correlated and increased significantly with activity level. Additionally, an increased stroke volume and ventilatory volume per minute were observed, followed by a mantle hyperinflation process during high activity periods. Squid metabolic rates dropped more than 75% during exposure to hypoxia. Maximum metabolic rates were not achieved under such conditions and the metabolic scope was significantly decreased. Hypoxia changed the relationship between mantle contraction strength and frequency from linear to polynomial with increasing activity indicating that, under hypoxic conditions, the jumbo squid primarily increases the strength of mantle contraction and does not regulate its frequency. Under hypoxia, jumbo squids also showed a larger inflation period (reduced contraction frequency) and decreased relaxed mantle diameters (shortened diffusion pathways), which optimize oxygen extraction efficiency (up to 82%/34%, without/with consideration of 60% potential skin respiration). Additionally, they breathe “deeply”, with more powerful contractions and enhanced stroke volume. This deep-breathing behavior allows them to display a stable ventilatory volume per min, and explains the maintenance of the squid’s cycling activity under such O2 conditions. During hypoxia, the respiratory cycles were shorter in length but increased in frequency. This was accompanied by an increase in the number of escape-jets during active periods and a faster switch between swimming modes. In late hypoxia (onset ~170±10 min), all the ventilatory processes were significantly reduced and followed by a lethargic state, a behavior that seems closely associated with the process of metabolic suppression and enables the squid to extend its residence time in the OMZ.