Metabolic costs imposed by hydrostatic pressure constrain bathymetric range in the lithodid crab Lithodes maja

Abstract

The changing climate is shifting the distributions of marine species, yet the potential for shifts in depth distributions is virtually unexplored. Hydrostatic pressure is proposed to contribute to a physiological bottleneck constraining depth range extension in shallow-water taxa. However, bathymetric limitation by hydrostatic pressure remains undemonstrated, and the mechanism limiting hyperbaric tolerance remains hypothetical. Here, we assess the effects of hydrostatic pressure in the lithodid crab (bathymetric range 4-790 m depth, approximately equivalent to 0.1 to 7.9 MPa hydrostatic pressure). Heart rate decreased with increasing hydrostatic pressure, and was significantly lower at ≥10.0 MPa than at 0.1 MPa. Oxygen consumption increased with increasing hydrostatic pressure to 12.5 MPa, before decreasing as hydrostatic pressure increased to 20.0 MPa; oxygen consumption was significantly higher at 7.5-17.5 MPa than at 0.1 MPa. Increases in expression of genes associated with neurotransmission, metabolism and stress were observed between 7.5 and 12.5 MPa. We suggest that hyperbaric tolerance in may be oxygen-limited by hyperbaric effects on heart rate and metabolic rate, but that 's bathymetric range is limited by metabolic costs imposed by the effects of high hydrostatic pressure. These results advocate including hydrostatic pressure in a complex model of environmental tolerance, where energy limitation constrains biogeographic range, and facilitate the incorporation of hydrostatic pressure into the broader metabolic framework for ecology and evolution. Such an approach is crucial for accurately projecting biogeographic responses to changing climate, and for understanding the ecology and evolution of life at depth.

NMDA Receptor Regulation Is Involved in the Limitation of Physiological Tolerance to Both Low Temperature and High Hydrostatic Pressure

“…Wittmann et al, 2010;Brown, 2015) and is reported in colder waters (0 • C) than Southern Ocean lithodids (0.2 • C) (cf. Hall and Thatje, 2011;Brown et al, 2017). Consistent with this hypothesis, heart rate is greater in L. maja than in the sub-Antarctic lithodid Paralomis granulosa at 0.1 MPa and 6 • C; respectively ∼28 bpm and ∼21 bpm at rest (Wittmann et al, 2012).…”

“…Hyperbaric tolerance in L. maja is also limited by hyperbaric effects on heart rate (Brown et al, 2017). Decreasing heart rate observed in L. maja in response to increasing hydrostatic pressure is similar to the decrease in heart rate observed in P. granulosa in response to decreasing temperature, suggesting that [Mg 2+ ] regulation may also critically influence hyperbaric performance.…”

“…Decreasing heart rate observed in L. maja in response to increasing hydrostatic pressure is similar to the decrease in heart rate observed in P. granulosa in response to decreasing temperature, suggesting that [Mg 2+ ] regulation may also critically influence hyperbaric performance. Linear regression indicates that heart rate decreases by 1.01 bpm • C −1 in P. granulosa (Wittmann et al, 2012) and by 0.889 bpm MPa −1 in L. maja (Brown et al, 2017). Disparity between hydrostatic pressure thresholds in relatively effective and ineffective haemolymph [Mg 2+ ]-regulating crustaceans supports this interpretation.…”

“…The physiological concept of oxygen-and capacity-limited thermal tolerance describes a mechanism where temperature tolerance is constrained by the ability to supply sufficient oxygen to meet metabolic demand (Pörtner, 2010). Recent experimental evidence indicates that hyperbaric tolerance is oxygen-and capacity-limited, too (Brown et al, 2017). However, whether the same fundamental mechanism limits both temperature and hydrostatic pressure tolerance, and what that mechanism may be, remains uncertain.…”

“…The hyperbaric decrease in L. maja's heart rate may also be mediated by depressed neurotransmission, resulting from shifts in NMDA receptor activity (Brown et al, 2017). Indeed, pressure depresses synaptic transmission at all examined synapses in shallow-water taxa (see Aviner et al, 2010), including the crustacean neuromuscular junction (Campenot, 1975).…”