Development of Embryonic Market Squid, Doryteuthis opalescens, under Chronic Exposure to Low Environmental pH and [O2]

Abstract

The market squid, Doryteuthis opalescens, is an important forage species for the inshore ecosystems of the California Current System. Due to increased upwelling and expansion of the oxygen minimum zone in the California Current Ecosystem, the inshore environment is expected to experience lower pH and [O2] conditions in the future, potentially impacting the development of seafloor-attached encapsulated embryos. To understand the consequences of this co-occurring environmental pH and [O2] stress for D. opalescens encapsulated embryos, we performed two laboratory experiments. In Experiment 1, embryo capsules were chronically exposed to a treatment of higher (normal) pH (7.93) and [O2] (242 μM) or a treatment of low pH (7.57) and [O2] (80 μM), characteristic of upwelling events and/or La Niña conditions. The low pH and low [O2] treatment extended embryo development duration by 5–7 days; embryos remained at less developed stages more often and had 54.7% smaller statolith area at a given embryo size. Importantly, the embryos that did develop to mature embryonic stages grew to sizes that were similar (non-distinct) to those exposed to the high pH and high [O2] treatment. In Experiment 2, we exposed encapsulated embryos to a single stressor, low pH (7.56) or low [O2] (85 μM), to understand the importance of environmental pH and [O2] rising and falling together for squid embryogenesis. Embryos in the low pH only treatment had smaller yolk reserves and bigger statoliths compared to those in low [O2] only treatment. These results suggest that D. opalescens developmental duration and statolith size are impacted by exposure to environmental [O2] and pH (pCO2) and provide insight into embryo resilience to these effects.

Dose-dependence and small-scale variability in responses to ocean acidification during squid, Doryteuthis pealeii, development

“…Doryteuthis opalescens egg capsules cultured under decreased pH (pH 7.57, pCO 2 ~1440 ppm) and hypoxia (80 µM O 2 ) also showed delays in embryogenesis (Navarro et al 2016). Further, this study suggested that the combination of these stressors, potentially driven by the hypoxia, resulted in smaller embryonic statoliths, the aragonitic structures responsible for the squid's sensing of balance, orientation, and sound (Navarro et al 2016).…”

Oceanographic influences on the distribution and relative abundance of market squid paralarvae (Doryteuthis opalescens) off the Southern and Central California coast

“…Warmer waters can shift fisheries north or into deeper offshore waters where they are not harvestable. The inshore environment in the CCE is also expected to suffer from lower pH and oxygen availability, further stressing market squid populations (Navarro et al., ). Ecosystem alternations due to climate change can affect the timing of the fishery and industry operations and reduce the standing stock, potentially costing millions in lost revenue.…”

“…The fishery for market squid is routinely one of the largest and most valuable in the state of California (Leos, ). Market squid disperse over the continental shelf as juveniles and form dense nearshore spawning aggregations when mature, depositing eggs into clusters over shallow, sandy substrate (Navarro et al., ; Zeidberg & Hamner, ). The commercial fishery generally targets these spawning aggregations during summer in the Monterey Bay region (MBR), and during fall in the Southern California Bight (SCB, Figure ; Zeidberg, Hamner, Nezlin, & Henry, ), although spawning has been observed year round in some instances (Fields, ; Jackson & Domeier, ; Navarro, ).…”

“…eggs into clusters over shallow, sandy substrate (Navarro et al, 2016;Zeidberg & Hamner, 2002). The commercial fishery generally targets these spawning aggregations during summer in the Monterey Bay region (MBR), and during fall in the Southern California Bight (SCB, Figure 1; Zeidberg, Hamner, Nezlin, & Henry, 2006), although spawning has been observed year round in some instances (Fields, 1950;Jackson & Domeier, 2003;Navarro, 2014).…”

Physiological and ecological implications of ocean deoxygenation for vision in marine organisms

“…Embryonic visual development is vital to survival upon hatching; for example, some cephalopods develop the ability to discern contrast or learn to identify copepod prey during embryogenesis [140,141]. Hypoxia is known to cause developmental delays, mortality and/or morphological deformities in frogs [142], gastropods [138], abalone [143], brachyuran crabs [144] and squid [145,146]. Hypoxiainduced impairments to visual system development in marine organisms include a reduction in the size of the eyespot in the mussel (Mytilus edulis [147]) and eye deformities in hatched squid paralarvae (Sepioteuthis australis), potentially from lower oxygen found in capsules at the centre of egg clusters in comparison to those on the outside of the group [148].…”