less stimulation was required to elicit neural activity in isolated nerve preparations in both species when they were under low pressure. Their results failed to explain the observed moribundity at high pressures, nor did they give a mechanistic explanation for why neural stimulation occurred at modest pressures.
Campenot used a neuromuscular preparation of the walking legs of two Crustacea to evaluate the effects of pressure. The first preparation was from Homarus americanus, the New England lobster dwelling in water 520 m and shallower. The other was of Chaceon (formerly Geryon) quinquidens, a deeper‐dwelling red crab found from 300 to 1600 m on the continental slopes of coastal North America. Dr. Campenot’s technique was straightforward; he stimulated the excitatory neuron leading to the muscle with one electrode and recorded the response from the muscle with another.
Figure 2.17 The effect of pressure on Excitatory Junction Potentials (EJP) recorded from a lobster muscle fiber. Each bar represents the average of about 20 EJP's. The ordinate is an amplitude index with the first average at 1 atm for each frequency set at 1. Its value in millivolt is given in parenthesis.
Source: Adapted from Campenot (1975), figure 3 (p. 136). Reproduced with the permission of Elsevier.
Muscles respond to neural excitation with Excitatory Junction Potentials (EJPs) which then effect a muscle contraction. By examining the amplitude of the EJPs in response to a given fixed stimulus at different hydrostatic pressures, the effect of pressure on the neuromuscular response could be described. Dr. Campenot found that pressure caused an across‐the‐board depression of EJP amplitude in the lobster (Figure 2.17), but the EJP amplitude was independent of pressure in the deeper‐dwelling red crab. In fact, it is now known that independence from pressure effects in species that dwell under pressure is the most common adaptive strategy.
The postulated cause for EJP depression in lobster was a pressure‐induced interference of neurotransmitter release at the synapse. At virtually all junctions between nerve and muscle, the neural signal is propagated across the microscopic gap at the neuromuscular junction using a chemical, or neurotransmitter, the best known of which is acetylcholine. Both excitatory and inhibitory neurotransmitters are present at the neuromuscular junction. It was speculated that the observed stimulatory effects of modest pressure were caused by a differential inhibition of transmitter release at inhibitory synapses. In such a situation, excitatory neural activity would then greatly over‐ride the depressed inhibitory synapses, resulting in hyperactivity.
Whole Animal Work
The first study of pressure effects on an animal normally living under pressure was that of Napora (1964) who tested pressure effects on the vertically migrating prawn Systellaspis debilis. In the western Atlantic, where Napora did his work, Systellaspis resides between depths of 500 and 1800 m during the day and 300 and 350 m at night. Napora found that increased pressure resulted in an increased metabolism (measured as oxygen consumption rate) between temperatures of 3 and 20°C and pressures of 0 and 1500 psi. The conclusion from his study was that increases in metabolism as a result of pressure effects offset the decline in metabolism due to the lower temperatures at daytime depth, resulting in a more constant metabolic rate over the diel cycle.
Two additional studies, Teal and Carey (1967) and Teal (1971), improved on Napora’s original work, also using species from the northwestern Atlantic. In the first study, the effects of pressure between 0 and 1000 atm were tested on a suite of migrating euphausiids, shrimplike Crustacea 10–25 mm in size found in pelagic waters throughout the world ocean (Chapter 7). The physiological process monitored was once again oxygen consumption rate. Measurements took place at temperatures between 5 and 25 °C, which are typical of the species’ vertical range. Oxygen consumption rate (VO2) was monitored continuously with an oxygen electrode as individuals were rapidly compressed, allowed to remain at pressure for 15–30 minutes, then decompressed. Temperature and pressure were both changed acutely, i.e. without allowing the animal time to acclimate to either variable. Several species of euphausiids were tested in this manner, most of which were epipelagic migrators that came to or near surface waters at night from daytime depths of 200 to 500 m. The rationale for acute measurements was that animals experiencing rapid temperature and pressure changes in the field would be fine with similar treatment in the laboratory, an assumption which was experimentally verified.
The results of the first study (Figure 2.18) showed a different response to pressure in epipelagic migrators (e.g. Euphausia hemigibba) than in the mesopelagic migrators (Thysanopoda monocantha) that did not go to the upper 50 m of the water column during their nightly migration. Pressure showed no significant effect on metabolism in epipelagic migrators at pressure and temperatures typical of their normal environment. Pressure increased VO2 only when experimental temperatures and pressures were out of synchrony with those in their normal environment. That is, pressure had no effect unless the pressure–temperature combinations were those that the animals would never normally encounter. In the mesopelagic migratory species Thysanopoda monocantha, pressure increased VO2 enough to offset some of the effects of the lower temperature of their daytime depth such that VO2 remained fairly constant the animal’s normal depth range.
Figure 2.18 Respiration of euphausiids plotted against depth using the indicated depth‐temperature distribution, which is typical of summer open‐ocean conditions. The solid symbols indicate respiration determined solely by temperature. Where pressure has a significant effect, an open symbol includes the effect of both factors.
Source: Adapted from Teal and Carey (1967), figure 5 (p. 730). Reproduced with the permission of Elsevier.
The study’s overall conclusions were that
1 Temperature alone determines VO2 in epipelagic vertical migrators
2 Temperature and pressure working in tandem in mesopelagic vertical migrators make VO2 more constant over the vertical range of the species.
Teal’s 1971 follow‐up study dealt with pressure effects on migrating mesopelagic decapod crustaceans, including Systellaspis debilis, the experimental species of Napora (1964). His results were similar to those of Napora and to his own 1967 study on euphausiids: pressure increased VO2 in the vertically migrating mesopelagic species resulting in a more stable VO2 over their vertical range. Thus, three studies supported conclusion number 2 above. We can add a third conclusion from work on non‐migrating mesopelagic species: pressure has little or no effect on the VO2 of non‐migratory mesopelagic species (Meek and Childress 1973).
Molecular Mechanisms of Adaptation to Pressure
The fact that deeper‐living species seemed insensitive to pressure piqued the curiosity of biochemical physiologists seeking a molecular basis for the observed data. Using the enzymatic reactions of intermediary metabolism as an experimental system, several studies explored the effects of pressure on deeper‐living species. Their a priori reasoning took them back to the basic thermodynamic properties of chemical reactions, which are governed not only by temperature and the concentration of reactants but also by differences in the volume of the reaction system when reactants are changed into products.
1 If