Ecophysiology of Oxygen Supply in Cephalopods

Cephalopods are an important component of many marine ecosystems and support large fisheries. Their active lifestyles and complex behaviors are thought to be driven in large part by competition with fishes. Although cephalopods appear to compete successfully with fishes, a number of their important physiological traits are arguably inferior, such as an inefficient mode of locomotion via jet propulsion and a phylogenetically limited means of blood-borne gas transport. In active shallow-water cephalopods, these traits result in an interesting combination of very high oxygen demand and limited oxygen supply. The ability to maintain active lifestyles despite these metabolic constraints makes cephalopods a fascinating subject for metabolic physiology. This dissertation focuses on the physiological adaptations that allow coleoid cephalopods to maintain a balance of oxygen supply and demand in a variety of environmental conditions. A critical component of understanding oxygen supply in any animal is knowing the means of oxygen delivery from the environment to the mitochondria. Squids are thought to obtain a fairly large portion of their oxygen via simple diffusion across the skin in addition to uptake at the gills. Although this hypothesis has support from indirect evidence and is widely accepted, no empirical examinations have been conducted to assess the validity of this hypothesis. In Chapter 2, I examined cutaneous respiration in two squid species, Doryteuthis pealeii and Lolliguncula brevis, by using a divided chamber to physically separate the mantle cavity and gills from the outer mantle surface. I measured the oxygen consumption rate in the two compartments and found that, at rest, squids only obtain enough oxygen cutaneously to meet demand of the skin tissue locally (12% of total). The majority of oxygen is obtained via the traditional branchial pathway. In light of these findings, I re-examine and discuss the indirect evidence that has supported the cutaneous respiration hypothesis. Ocean acidification is believed to limit the performance of squids due to their exceptional oxygen demand and pH-sensitivity of blood-oxygen binding, which may reduce oxygen supply in acidified waters. The critical oxygen partial pressure (Pcrit), defined as the PO2 below which oxygen supply cannot match basal demand, is a commonly reported index of hypoxia tolerance. Any CO2-induced reduction in oxygen supply should be apparent as an increase in Pcrit. In Chapter 3, I assessed the effects of CO2 (40 to 140 Pa) on the metabolic rate and Pcrit of two squid species: Dosidicus gigas and Doryteuthis pealeii. Carbon dioxide had no effect on metabolic rate or hypoxia tolerance in either species. Furthermore, considering oxygen transport parameters (e.g. Bohr coefficient, blood P50) and blood PCO2 values from the literature, I estimated an increase in seawater PCO2 to 100 Pa (≈1000 μatm/ppmv) would result in a maximum drop in hemocyanin-O2 saturation by 6% at normoxia and a Pcrit increase of ≈1 kPa (≈5% air saturation) in the absence of active extracellular pH compensation. Such changes are unlikely given the capacity for acid-base regulation in many cephalopods. Moreover, this estimated change is within the 95% confidence intervals of the Pcrit measurements reported here. Squid blood-O2 binding is more sensitive to pH than most other marine animals measured to date. Therefore, the lack of effect in squids suggests that ocean acidification is unlikely to have a limiting effect on blood-O2 supply in most marine animals. The pelagic octopod, Japetella diaphana, is known to inhabit meso- and bathypelagic depths worldwide. Across its range, individuals encounter oxygen levels ranging from nearly air-saturated to nearly anoxic. In Chapter 4, we assessed the physiological adaptations of individuals from the eastern tropical Pacific (ETP) where oxygen is extremely low. Ship-board measurements of metabolic rate and hypoxia tolerance were conducted and a metabolic index was constructed to model suitable habitat for aerobic metabolism. I found that animals from the ETP had a higher metabolic rate than animals from more oxygen-rich habitats. Despite their higher oxygen demand, they maintained better hypoxia tolerance than conspecifics from oxygen-rich Hawaiian waters. Furthermore, I found that hypoxia tolerance in Japetella has a reverse temperature dependence from most marine ectotherms, a characteristic that uniquely suits the physical characteristics of its oxygen-poor environment. Even with their high tolerance to hypoxia, the OMZ core likely has insufficient oxygen supply to meet the basal oxygen demand of Japetella. Despite the limited aerobic habitat in this region, species abundance was comparable to more oxygenated ocean regions, suggesting that physiological or behavioral plasticity such as altered hypoxia tolerance or hypoxic avoidance in this globally-distributed species is sufficient to maintain species fitness in this extreme environment. These findings contribute towards our understanding of the impacts of climate change on cephalopod physiology and biogeography. The study of environmental physiology provides a mechanistic basis for the understanding and prediction of ecological responses to climate change