Comp. Biochem. Physiol. Vol. 116A, No. 4, pp. 291–297, 1997 ISSN 0300-9629/97/$17.00Copyright 1997 Elsevier Science Inc. PII S0300-9629(96)00354-4

REVIEW

Hydrostatic Pressure as an Environmental Factorin Life Processes

A. G. MacdonaldDepartment of Biomedical Sciences, Marischal College, University of Aberdeen,

Aberdeen, AB9 1AS Scotland, U.K.

ABSTRACT. Hydrostatic pressure exists in all biological environments. In the deep sea the high pressure (upto approximately 100 MPa) has elicited molecular modifications in the organisms adapted to live there. Studyingthese is not particularly easy but a theoretical physical–chemical basis exists. Locomotor activity and behaviourare particularly sensitive to pressure and the most critical adaptations to high pressure appear to occur in thenervous system, although they are still obscure. In contrast, the effects of micro-pressures (,kPa) manifest inthe physiology of certain cells and the behaviour of many animals, which lack a gas phase, appear too small toarise from orthodox chemical reactions in solution. One particular micro-pressure sensor being studied in thecrab statocyst appears to use the principle of the dilatometer, converting a bulk volume change into a lineardisplacement. Since some cells also respond to micro-pressure changes the question arises, is there an intracellularmicro-pressure sensor and does it too work like a dilatometer? Copyright 1997 Elsevier Science Inc. comp bio-

chem physiol 116A;4:291–297, 1996.

KEY WORDS. High pressure, micro-pressure, hydrostatic pressure, deep sea, sensory physiology, Crustacea

I. INTRODUCTION high hydrostatic pressure of deep water has been studied at(i) Environments the cellular, kinetic and molecular levels, using orthodox

biochemical and physiological preparations and methods,Hydrostatic pressure, as distinct from high hydrostatic pres-in conjunction with less familiar high pressure techniquessure, is present in all biological environments. In air theand thermodynamic analysis (41). In contrast, the study ofpressure is typically close to normal atmospheric pressure atthe responses of animals and cells to very small changes insea level but it decreases with increase in altitude, simulta-hydrostatic pressure has been largely confined to experi-neously changing the partial pressure of constituent gases.ments seeking to characterise the response. The study ofIn the case of aquatic environments there are three mainthe mechanisms by which such micropressure changes aretypes: marine and freshwater, geothermal fluids and miscel-transduced is in its infancy.laneous microenvironments. Some of the points to be made

Generally, macroscopic aquatic environments present aconcerning low hydrostatic pressures may also apply to gas-linear pressure gradient, with pressure increasing by one at-eous environments.mosphere each 10 m of water column. Geothermal fluidsThe familiar aquatic environments present the full rangeincluding aquifers and oil well brines, also present a depth-of hydrostatic pressure, from micro-pressures generated byrelated increase in pressure but one that is complicated bya few centimeters of water column to approximately 1100gas pressures and geological conditions and often accompa-atmospheres in the deepest ocean trenches. The latter, highnied by high temperatures. For example in the biggest oilhydrostatic pressures are effectively constant at any fixedfield in the North Sea, the Forties field, the pressure reachesdepth whereas the small or micro-pressures experienced by22 MPa and the temperature 90°C (19,43). Artificially in-organisms may vary, with the tide or wave height forexample.troduced microorganisms exist in oil well brines but thereThe adaptation of animals and microorganisms to theis an intriguing possibility that a natural flora exists inde-pendently of surface life (16).

Presented in part at a symposium on ‘‘Life in Extreme Environments’’ at Microenvironments include skeletal load-bearing jointsLa Seyne-sur-Mer, France (June, 1995), sponsored by the European Society

of vertebrates in particular, which contain regions in whichof Comparative Physiology & Biochemistry.Address reprint requests to: A. G. Macdonald, Department of Biomedical hydrostatic transients occur. In the case of the human hip

Sciences, c/o Zoology Building, University of Aberdeen, Tillydrone Ave- joint for example, 10–20 MPa has been measured (13).nue, Aberdeen AB24 2TZ, Scotland, U.K. Tel. 01224-272399; Fax 01224-

Body fluids in general also exert a small hydrostatic pressure,272396.Received 9 March 1996; accepted 11 June 1996. giving rise to the pressure differential across permeable bar-

292 A. G. Macdonald

riers such as blood vessel walls, or to fluid gradients that term need not be very large for ∆G to be affected. Hencethe rate or equilibrium constant of many reactions will beresult in bulk flow, as in the blood stream or lymph ducts.

There also occurs a local shear stress at the interface be- affected and reactions will proceed faster or slower, de-pending on the sign of ∆V. A positive ∆V causes an in-tween the flowing fluid and the substrate in, for example,

arteries. However there is evidence that the hydrostatic creased hydrostatic pressure to reduce a reaction rate andvice versa.pressure that accompanies these dynamic factors may exert

a third, distinctive effect on the cells confining the fluid The kinetic analysis of high-pressure effects in biochemi-cal or physiological systems is generally based on rate pro-pressure (see section III). The hydrostatic pressure term is

very small, in the millibar range, comparable to that which cess theory. The real difficulties lie in dissecting out thecritical rate-limiting components and isolating co-variables.is sensed by aquatic animals mentioned earlier. Similarly

there is a difficulty in understanding how cells might be There exists a body of knowledge of how pressures effectstructural and enzymic proteins (12), lipid bilayers (20 andaffected by (transduce) such small pressures, an issue which

will be expanded later in this article. Finally for the sake of for very high pressures, 51), enzyme reactions (40,42) and,in less detailed fashion, complicated integrated processescompleteness, microenvironments also include laboratory

centrifuge tubes, in which a significant hydrostatic pressure such as muscle contraction and the conduction of actionpotentials (See the multi-author review, 21).occurs as a function of speed, radius, water column depth

and density (48). High hydrostatic pressures are sometimes In contrast to high hydrostatic pressure, low or micro-hydrostatic pressure may be defined for present purposes asconveniently generated by centrifuging (4,36), although in

most laboratory work presses, pumps and intensifiers are the contributing a small P term in equation (1) such that ∆Vhas to be extraordinarily large for any significant change tonormal devices used for pressurising samples.

A final point to be made in this introduction concerns occur in ∆G. It will be argued that some of the responsesof aquatic animals (see section III) and tissue cells to micro-the units used to express pressure. The S.I. nomenclature

has its limitations and custom and practicalities favour the pressure changes imply that ∆V would have to be unreal-istically large if the P.∆V term is to assume a sufficientcontinued use of other units of pressure, particularly atmo-

spheres. Water depth and gas partial pressure (the gas being magnitude to change ∆G and hence exert an effect on anequilibrium or reaction rate. Alternatively mechanismseither dissolved or not) are often important co-variables in

this field, which confuses the reader further. The following other than those existing in conventional solution chemis-try have to be invoked. The presence of a bulk gas phase,relationships, some rounded, may be helpful. 1 atmosphere

5 1 bar 5 1000 mbars 5 1000 cm H2O 5 76.0 cm Hg 5 either in macroscopic or microscopic form, is an obviouspossibility but many cases are known in which no gas phase100 KPa 5 0.1 MPa, the last two being S.I. units. A given

pressure invariably means above normal atmospheric pres- appears to be present (8), implying the existence of novellow pressure transducing systems.sure, but to be quite unambiguous a pressure of, for example,

0.1 atm, can be expressed as 1.1 atm absolute. This paper deals with both high and micro-pressures. Inthe former case the behavioural responses of animals areemphasised because they appear to provide a continuum

(ii) Thermodynamics and Kinetics with the behavioural responses to micropressures. In the lat-Whatever the magnitude of hydrostatic pressure and how- ter case the effects of micro-pressures on both organismsever short lived it may be as a pulse, or prolonged as a per- and cells are described and the thermodynamic implicationsmanent environmental feature, its effect on a reaction sys- considered.tem is conventionally analysed using these fundamentalrelationships (3,7):

II. EFFECTS OF HIGH HYDROSTATICPRESSURE: DEEP SEA ANIMALS∆G 5 ∆H 2 T∆S

(1)5 (P∆V 1 ∆E) 2 T.∆S The deep sea, the largest of biological environments, is in-habited throughout its pressure range (100 to nearly 1100atm) by animals and bacteria that are assumed to be adapted1d ln k

dp 2T

52∆VRT

(2)to their ambient pressure. Much effective work can be car-ried out on material extracted at sea from freshly collectedanimals, and subsequently investigated in a normal labora-This means that, at constant temperature, an equilibrium

constant (or rate constant) is affected by pressure through tory. There exists an extensively reviewed body of biochem-ical knowledge of the effects of deep sea pressures on en-the P.∆V term in the free energy (∆G) term in equation

(1). ∆H, ∆S and T have their usual meaning. Thus the mo- zymes, other proteins and on bilayer lipids thus extractedfrom deep sea organisms (see above). In a number of caseslar volume change (∆V) and the pressure (P) combine to

alter ∆G. When P is in the MPa range, (say 5 to thousands, there is evidence that specific macromolecules are adaptedto the high pressures normally experienced.the latter of interest in high-pressure chemistry) the ∆V

Hydrostatic Pressure as an Environmental Factor in Life Processes 293

But what direct evidence is there that deep sea animals from Lake Baikal (Table 1B). (C) Many crustacea appeardead after collection from a significant depth but resumeare actually adapted to their high pressure? The vertical zo-

nation established by ecologists for a number of species im- normal activity on being restored to a pressure similar tothat from which they have been collected. Pressure-resusci-plies adaptation to a specific pressure range, implying that

deep sea animals might be adapted to function normally tation may take minutes or hours (Table 1,C). (D) The life-less appearance on collection arises fairly late in the decom-only within a specific range of high pressure. The obvious

way to examine this implication of pressure tolerance is to pression profile and has been directly observed inamphipods collected in isobaric traps, and in one case filmedcollect animals from specific depths and subject them to

appropriate pressure tests, monitoring their activity. during the ascent of a simple, non-pressure retaining trap(Table 1D). (E) Perhaps the most obvious evidence of high-It is a remarkable fact that although the susceptibility of

shallow water animals to high (i.e. deep sea) pressures was pressure tolerance is the normal activity of deep sea animalsat pressures that paralyse their shallow-water counterparts.established in the 1870s it was only in the 1970s that com-

parable pressure experiments were carried on deep water an- Such activity has been seen from submersible craft, andfilmed by cameras lowered from the surface, and directlyimals, to ascertain their short-term tolerance to decompres-

sion and to high pressure (17,18,28,33). observed in isobaric traps (Table 1,E).These criteria of high-pressure tolerance show the ner-Shallow water animals respond to gradually applied hy-

drostatic pressures with a series of changes in their motor vous and muscular systems of deep sea animals to be animportant site of adaptation. We have no idea how suchactivity. There is an initial increase in normal activity dur-

ing the first few atmospheres of compression, followed by a adaptation is achieved but clearly the problem requires theexcitable properties of deep sea nerve and muscle to be stud-phase of impaired coordination in otherwise normal behav-

iour. Excitability increases with pressure, culminating in the ied. Some preliminary experiments have been published(5,14,32,47).region of 100 atm in spasms or convulsions. In the case of

decapod crustacea with a ‘‘tail-flip’’ escape reflex, this is of-ten triggered early on and, in distorted form, is the focus of

III. EFFECTS OF MICRO-PRESSURES: AQUATICviolent convulsive behaviour at higher pressures. In the caseANIMALS AND CELLS

of amphipods, relatively slow dorsally directed spasms of thelongitudinal musculature occur at high pressure. At pres- Fish with a gas-filled swim bladder have an ingenious device

for regulating their buoyancy and also one which appearssures higher than those that elicit spasms or convulsions,a progressive immobilisation sets in, reversibly at first, but well suited to detect small changes in ambient hydrostatic

pressure. The bulk compressibility of the gas within theeventually irreversibly.This pattern provides a behavioural basis for studying the bladder (31) readily translates into a linear displacement of

the confining wall. Aquatic insect larvae use their air-filledpressure tolerance of deep sea animals, with the corollarythat such animals are liable to be adversely affected during trachea to provide buoyancy but they sense a state of nega-

tive buoyancy by detecting water currents associated withtheir collection. Small crustacea are relatively hardy in thisrespect, and also are the only type of animal to be collected sinking and inflate their buoyancy chamber to compensate

(44). However many aquatic animals which lack an obviousin isobaric traps (i.e. brought to the surface at their normalambient, high pressure) (22,25,52). Observations have also gas phase also respond to very small changes in hydrostatic

pressure, see for example (34) and (9). In the case of thebeen made on amphipods and other aquatic animals, in-cluding fish, brought to the surface in simple traps or trawls, larvae of the crab Rhithropanopeus harrisii, the minimum step

pressure change able to induce a behavioural response is 13and therefore subjected to hydrostatic decompression, andother trauma such as an increase in temperature and light. mbar (i.e. 0.003 atm or 0.3 KPa, or an increase of 3 cm in

the height of a water column) or 28 mbar (i.e. a pressureOur current knowledge is clearly incomplete but several in-teresting criteria of pressure tolerance have emerged from decrease). Responses to continuous pressure changes are

comparably sensitive; the passive sinking of the same larvaethe experimental reports. Most observations have beenmade on crustacea and are summarised in Table 1. The induces an ascent response (9). In darkness larvae respond

to a pressure increase of 0.175 mbar s21 with increased swim-analogous information on fish is given in (35).The criteria are as follows. (A) Some crustacea can be ming and negative geotaxis.

These values present a clear problem; how do such organ-collected from moderate depths without drastic impairmentof their locomotor activity, and when subjected to an in- isms detect these micro-pressures and how is the detection

(transduction) related to the animals’ neuro-muscular sys-creased stepwise pressure test show no hyperexcitability atany stage, unlike shallow water species (Table 1A). At tem and behaviour? Before examining this question the mi-

cro-pressure effects on cultured cells should be considered.higher pressure their activity is reduced. (B) Others, whensubjected to a stepwise pressure increase show a significantly First, bovine pulmonary artery endothelial cells, grown

in culture, apparently release a fibroblast growth factor intohigher convulsion threshold pressure than their shallow wa-ter counterparts, and these include freshwater amphipods the medium when subjected to 1.5–15 cm water pressure,

294 A. G. Macdonald

TABLE 1. The high-pressure tolerance of deep sea crustacea and other invertebrates based on behavioural, motor activity

A. No hyperexcitability at increased pressure

Depth of collection, mAnimal Depth range, m and references

Gigantocypris mulleri (Ostracoda) 260–2300 Less than 1500 (17,23)Cirolana borealis (Isopoda) — 680 (28)Munida gracilepes (Decapoda) — 680 (28)Lanceola sayana (Amphipoda) — Less than 1500 (24)Eurythenes gryllus (Amphipoda) 1000–6200 1850 (11)

B. Convulsions and other excitable activity caused by very high pressure

AmphipodaParalicella capresca Orchomene sp. (mild hyperexcitability at 500–700 atm) 4000 (26)Tmetonyx cicada, Eurythenes sp. (convulsions at 250–450 atm) 1300 & 2000 (25)Acanthogammarus grewinki and other Lake Baikal species (convulsions at 150–

190 atm compared with 90 atm for shallow water species) .1000 m (2)

C. Decompression paralysis during collection; subsequent resuscitation on recompression

Munnopsis typica (Isopoda) — 680 (28)Rhizocrinus lofotensis (Crinoid) — ′′ ′′Dentalium sp. (Scaphopoda) — ′′ ′′Aglasphemia bispinosa (Hydrazoa) — ′′ ′′Tmetonyx cicada (Amphipoda) — 1200 (25)Eurythenes sp. (Amphipoda) — 2000 ′′Bythograea thermydron (Brachyura) — 2500 (29)Paralicella capresca (Amphipoda) — 4000 (26)Eurythenes grillus (Amphipoda) — 4000 ′′

Unidentified amphipods 5700 m (52)

D. Decompression paralysis observed in amphipods under controlled conditions

(i) decompression after re-compression resuscitation.Paralicella capresca and other species 4300 (26)

(ii) decompression in isobaric trap, starting at 600 atm. Immobilization at 300, 215 atm (52,53)(iii) decompression filmed in a trap containing amphipods, ascending from 4855 m; immobilization at 160–180 atm (45)

E. Normal activity at high pressure

Benthic amphipods collected in isobaric traps and observed at their normal ambient pressure in a ship’s laboratory (25,27,52)Benthic amphipods filmed on the ocean floor

i.e. (1.5–15 mbar) for several days (1,39). When grown un- Finally, human platelets perform a remarkably complexaggregation process in vitro, which is preceded by the releaseder 0.3 cm of water (0.33 mbar) the release of the growth

factor is much reduced and its presence is apparent in both of a number of substances. A hydrostatic pressure of 260mbar enhances the release of platelet factor 4 and beta-the nucleus and the cytoplasm of the cultured cells. The

possibility has been considered, and rejected, that pO2, thromboglobulin, and increases the formation of malondial-dehyde (46). We need not be concerned with the complexi-pCO2 or pH might be the prime cause of these effects. As

a consequence of the enhanced release of the growth factor, ties of the aggregation reaction here; the point is that theplatelets appear to detect 260 mbar hydrostatic pressure.cells grown in the pressure range 1.5–15 mbar showed in-

creased proliferation and a loss of contact inhibition, mani- Somewhat higher pressures have also been used to perturbplatelet aggregation (13).fest as multiple layers of cells. Other endothelial cells, iso-

lated from human umbilical veins and grown in culture, Returning to the question of the nature of the micro-pressure transducers responsible for these effects, we shouldrelease nitric oxide when stimulated by histamine. Hishi-

kawa and colleagues (15) found that this release process was first consider the possibility that a gas micro-phase exists,since gas is highly compressible. Digby (6) proposed the ex-inhibited by 50 mbar (50 cm of a water column) or more

hydrostatic pressure, applied to the culture flask with helium istence of an electrically generated gas film on the surfaceof certain regions of crustacean cuticle, arguing that thisgas.

Hydrostatic Pressure as an Environmental Factor in Life Processes 295

could respond to very small pressure changes and in some on the limits of credibility, and far from being a practicalhypothesis.unspecified way, provide an input to the animals’ nervous

system. Enright (8) measured the bulk compressibility of Can the bulk compression of a solvent, water or perhapsa lipid phase, be sufficient to serve as a micro-pressure trans-crustacea and concluded that any bulk gas phase present

must be exceedingly small. Digby’s idea cannot easily be ducer? The small compressibility of liquids does not, at first,make this a likely possibility. 100 MPa decreases the volumerefuted but it has not attracted any support over the years.

We therefore have to examine the possibility that a volume of water by 4% and the volume of organic solvents by about14% (49). But consider the consequences of confining thechange can occur in a liquid, probably aqueous, system such

that pressures on the mbar scale will exert a significant effect bulk liquid in a narrow necked container, like a thermome-ter, or more generally, a dilatometer. The small bulk com-on some equilibrium or rate constant. For present purposes

we may distinguish two classes of volume change; one de- pression is converted to a significant linear displacementwithin the narrow section of the container. Such a devicerives from solute-solvent interactions, i.e. changes in the

partial molar volume of solutes; the other is the bulk com- might exist on an intracellular scale, or on a multi-cellularscale. It would also be extremely sensitive to temperaturepressibility of a liquid phase, i.e. a change in the molar vol-

ume of a solvent. Considering the first of these, what molar fluctuations; indeed the laboratory technique of precisiondilatometry is complicated by considerations of temperaturevolume change (∆V) is required for 1 KPa or 10 mbar, for

example, to change an equilibrium or rate constant 0.5%? control (50).The dilatometer principle may serve as the pressure trans-From equation (2) it may be shown that a ∆V of 104 ml

mol21 is required. Is such a ∆V physically possible? ducer in crabs, whose behavioural responses show they candetect pressure changes of less than 10 KPa (30). Here theConventional high-pressure experiments on several mac-

romolecules have revealed ∆V values that are very large in- focus of interest is the statocyst, the organ of balance.Thread hairs are displaced by inertial fluid movement in thedeed. For example, the Brome mosaic virus is dissociated by

pressure into 90 dimers, with an overall reaction volume statocyst canals. At the base of each hair there is a mechani-cal linkage (chorda) to a pair of neurones, which generatefor the dissociation of 22960 ml mol21 (37). The reaction,

however, cannot be regarded as a single process, associated– a train of action potentials whose frequency reflects the an-gular displacement of the hair. Fraser and colleagues (10)dissociated. Similarly the haemoglobin molecule from the

worm Glossoscolex paulistus is dissociated by high pressure, showed that a change in the ambient pressure of the stato-cyst isolated from Carcinus moenas affected the frequencyultimately to 96 monomeric units (38). The 1∆V per mol

of subunit association is 73 ml, hence the reaction volume of the train of spikes. The fine structure of the hair andchorda suggest a way in which this might arise. The chordafor the complete molecule is 17000 ml mol21. Significantly

the subunit interactions in these examples possess ∆V typi- appears to enter the base of the hair, which is hollowthroughout its length. Thus if the chorda behaves like acal of the values found in other protein interactions. The

volume change actually arises from the water molecules, piston, and the hair like a syringe barrel, then compressionof the fluid contents of the hair will cause a linear displace-which hydrate the protein subunits being more densely

packed than bulk water. However for a multimeric protein ment of the chorda, up the barrel. The diameter of a hairis typically 2 µm and the length 400 µm. Taking the com-to be so organised to respond to a pressure change of 10

mbar with a 0.5% shift in its equilibrium a ∆V of 104 ml pressibility of the fluid contents as 4.4 3 1027 bar21 then a0.2 bar pressure increase (i.e. 2 metres high water column)mol21, has to be thermodynamically coupled to the reaction

in question. The cooperativity required and the thermody- will cause the chorda to move .0035 µm. This is equivalentto the linear displacement of the chorda when the hair un-namic coupling are problematical and so too is the tempera-

ture stability of such a protein. Consider, instead of the arbi- dergoes an angular displacement close to its limit of sensitiv-ity. This is a plausible model of a micro-pressure transducer,trary change in rate or equilibrium constant of 0.5%

mentioned above, a change of 0.005%. The ∆V required to and many of its properties have yet to be explored andtested, not the least of which is its sensitivity to temperaturecause such a change on applying 10 millibars pressure is now

120 ml mol21, which is large but plausible. However, how fluctuations. Perhaps an intracellular transducer using thesame principle might be worth searching for in cells thatrealistic is it to invoke a perturbation of 0.005% in some

biochemical reaction rate or equilibrium? Reactions with a respond to micro-pressure changes.The conclusion, reached independently (1,15), that hy-Q10 of 2 imply that rates vary by 0.005% with a temperature

change of 0.0005°C, so our hypothetical pressure-sensitive drostatic pressures of 50 mbar or less affect cellular metabo-lism is highly suspect. The simple argument, given above,reaction is likely to experience large fluctuations due to

minute temperature changes, if it has the normal sensitivity shows that orthodox physical chemistry cannot sustain sucha conclusion. Yet a careful examination of the publishedto temperature. These would swamp any pressure effect.

For the present, the possibility that a molecular reaction reports leaves the reader with no obvious clues as to poten-tial artefacts or weaknesses in experimental design. The ef-in aqueous solution might underlie the sensitivity of aquatic

animals and culture cells to micro-pressures appears to be fects of somewhat higher micropressures (260 mbar) on

296 A. G. Macdonald

ral and artificial membranes. In: Balny, C.; Hayashi, R.; Here-platelets are equally intriguing (46). Is this a pressure effectmans, K.; Masson, P. (eds). High Pressure and Biotechnology.that arises from molecular reactions in solution, or is it to beColloque Inserm 224. London; U.K.: John Libbey and Co.

regarded as a micropressure effect? Clearly, micropressures 1992:67–75.present us with conceptually difficult and fascinating prob- 21. Macdonald, A.G. (ed). Effects of high pressure on biological

systems. Adv. Comp. Environ. Physiol. 17. Berlin, Germany:lems in diverse fields of physiology.Springer-Verlag; 1993.

22. Macdonald, A.G.; Gilchrist, I. Recovery of deep sea water atconstant pressure. Nature 222:71–72;1969.References

1. Acevedo, A.D.; Bowser, S.S.; Gerritsen, M.E.; Bizion, R. Mor- 23. Macdonald, A.G.; Gilchrist, I.; Teal, J.M. Some observationson the tolerance of oceanic plankton to hydrostatic pressure.phological and proliferative response of endothelial cells to

hydrostatic pressure: Role of fibroblast growth factor. J. Cell J. Mar. Biol. Assoc. U.K. 52:213–223;1972.24. Macdonald, A.G.; Teal, J.M. Tolerance of oceanic and shal-Physiology 157:602–614;1993.

2. Brauer, R.W.; Bekman, M.Y.; Keyser, J.B.; Nesbitt, D.L.; Side- low water crustacea to high hydrostatic pressure. Deep-sea Re-search 22:131–144;1975.ler, G.N.; Wright, S.L. Adaptation to high hydrostatic pres-

sures of abyssal gammarids from Lake Baikal in eastern Siberia. 25. Macdonald, A.G.; Gilchrist, I. Further studies on the pressuretolerance of deep-sea crustacea with observations using a newComp. Bicohem. Physiol. 65A:109–117;1980.

3. Bull, H.B. An Introduction to Physical Biochemistry. Phila- high pressure trap. Marine Biology 45:9–21;1978.26. Macdonald, A.G.; Gilchrist, I. Effects of hydraulic decompres-delphia: F.A. Davis Company; 1971:469.

4. Burkat, A.K.; Richard, A.J. Low-pressure studies of the iso- sion and compression on deep sea amphipods. Comp. Bio-chem. Physiol. 67A:149–153;1980.thermal compressibilities and specific volumes of organic liq-

uids. J. Chem. Thermodynamics 7:271–277;1975. 27. Macdonald, A.G.; Gilchrist, I. The pressure tolerance of deepsea amphipods collected at their ambient pressure. Comp. Bio-5. Campenot, R.B. The effects of high hydrostatic pressure on

transmission at the crustacean neuromuscular junction. chem. Physiol. 71A:349–352;1982.28. Menzies, R.J.; George, R.Y.; Paul, A.Z. The effects of hydro-Comp. Biochem. Physiol. 52B:133–140;1975.

6. Digby, P.S.B. Detection of small changes in hydrostatic pres- static pressure on living aquatic organisms. IV. Recovery andpressure experimentation on deep-sea animals. Int. Hydrobiol.sures by Crustacea and its relation to electrode action in the

cuticle. Symp. Soc. Exptl. Biol. 26:445–471;1972. 59:187–197;1974.29. Mickel, T.J.; Childress, J.J. Effects of pressure and temperature7. Edsall, J.T.; Gutfreund, H. Biothermodynamics. New York:

Wiley & Sons; 1983:248. on the EKG and heart rate of the hydrothermal vent crabBythograca thermydren (Brachyura). Biol. Bull. 162:70–82;8. Enright, J.T. Estimates of the compressibility of some marine

crustaceans. Limnol. Oceanog. 8:382–387;1963. 1982.30. Naylor, E.; Atkinson, R.J.A. Pressure and the rhythmic be-9. Forward, R.B.; Wellins, C.A. Behavioural responses of a larval

crustacea to hydrostatic pressure: Rhithropanopeus harrisii haviour of inshore marine animals. Symp. Soc. Exptl. Biol.26:295–415;1972.(Brachyura: Zanthidae). Marine Biology 101:159–172;1989.

10. Fraser, P.J.; Macdonald, A.G. Crab hydrostatic pressure sen- 31. Ona, E. Physiological factors causing natural variations inacoustic target strength of fish. J. Mar. Biol. Assoc. U.K. 7:sors. Nature 371:383–384;1994.

11. George, R.Y. What adaptive strategies promote immigration 107–127;1990.32. Pennec, J.P.; Wardle, C.S.; Harper, A.A.; Macdonald, A.G.and speciation in deep-sea environments? Sarsia 64:61–65;

1979. Effects of high hydrostatic pressure on the isolated hearts ofshallow water and deep sea fish; results of Challenger cruise12. Gross M.; Jaenicke, R. Proteins under pressure. Eur. J. Bio-

chem. 221:617–630;1994. 6B/85. Comp. Biochem. Physiol. 89A:215–218;1988.33. Regnard, P. Effect des hautes pressions sur les animaux marins.13. Hall, A.C.; Pickles, D.M.; Macdonald, A.G. Aspects of eu-

karyotic cells. In: Effects of High Pressure on Biological Sys- C.R. Sciences Soc. Biol. 36:394–395;1884.34. Reid, D.G.; Naylor, E. Entrainment of bimodal circatidaltems (chapter 2). Adv. Comp. Environ. Physiol. Berlin, Ger-

many: Springer-Verlag; 1993:29–85. rhythms in the shore crab Carcinus maenas. J. Biol. Rhythms5:333–347;1990.14. Harper, A.A.; Macdonald, A.G.; Wardle, C.S.; Pennec, J.P.

The pressure tolerance of deep sea fish axons. Results of Chal- 35. Sebert, P.; Macdonald, A.G. Fish. In: Effects of High Pressureon Biological Systems (chapter 5.) Adv. Comp. Environ.lenger cruise 6B/8S. Comp. Biochem. Physiol. 88A:647–653;

1987. Physiol. Berlin, Germany: Springer-Verlag; 1993:148–196.36. Seifert, T.; Bartholmes, P.; Jaenicke, R. High-pressure dissoci-15. Hishikawa, K.; Nakaki, T.; Suzuki, H.; Saruta, T.; Kato, R.J.

New method of investigating functional roles of pressure-sen- ation of the β2-dimer of tryptophan synthase from Escherichiacoli monitored by sucrose gradient centrifugation. FEBS Lett.sitive mechanoreceptor in human endothelial cells. Cardio-

vascular Pharmacol. 20 (suppl. 12):S66–S67;1992. 173:381–384;1984.37. Silva, J.L.; Weber, G. Pressure-induced dissociation of Brome16. L’Haridon, S.; Reysenbach, A.L.; Glenat, P.; Prieur, D.; Jean-

thon, C. Hot subterranean biosphere in a continental oil res- mosaic virus. J. Mol. Biol. 199:149–159;1988.38. Silva, J.L.; Villas-Boas, M.; Bonage, C.F.S.; Meirelles, N.C.ervoir. Nature 377:223–224;1995.

17. Macdonald, A.G. The role of high hydrostatic pressure in the Anomalous pressure dissociation of large protein aggregates.J. Biol. Chem. 264:15863–15868;1989.physiology of marine animals. Symp. Soc. Exptl. Biol. 26:209–

231;1972. 39. Sloan, C.M. The effects of elevated hydrostatic pressure oncultured endothelial cell morphology and transport properties.18. Macdonald, A.G. Physiological aspects of deep sea biology.

Cambridge, UK: Cambridge University Press; 1975. M.S. Thesis, Rensselaer Polytechnic Institute. Troy, NY;1990.19. Macdonald, A.G. Physiological adaptations to extreme pres-

sures: the implications for palaoecology. Trans. Roy. Soc. Ed- 40. Somero, G.N. Life at low volume change: hydrostatic pressureas a selective factor in the aquatic environment. Am. Zool.inburgh 80:263–270;1989.

20. Macdonald, A.G. Effects of high hydrostatic pressure on natu- 30:123–135;1990.

Hydrostatic Pressure as an Environmental Factor in Life Processes 297

41. Somero, G.N. Biochemical ecology of deep-sea animals. Expe- sea eel Histiobranchus bathybius. Results of Challenger cruise6B/85. Comp. Biochem. Physiol. 88A:595–598;1987.rientia 48:537–543;1992.

42. Somero, G.N. Adaptation to high hydrostatic pressure. Annu. 48. Wattiaux, R.; Wattiaux-De, C.; Ronveaux-Dupal, M.-F. Dete-rioration of rat liver mitochondria during centrifugation in aRev. Physiol. 54:557–577;1992.

43. Stetter, K.O.; Huber, R.; Blochli, E.; Kurr, M.; Eden, R.S.; sucrose gradient. Eur. J. Biochem. 22:31–39;1971.49. Weast, R.C. (ed). Handbook of Chemistry and Physics.Fielder, M.; Cach, H.; Vance, I. Hyperthermophilic archaea

are thriving in deep North Sea and Alaskan oil well reservoirs. Cleveland, Ohio: The Chemical Rubber Company; 1964.50. Wilkinson, D.A.; Nagle, J.F. A differential dilatometer. Anal.Nature 365:743–745;1993.

44. Teraguchi, S. Detection of negative buoyancy in the phantom Biochemistry 84:263–271;1978.51. Wong, P.T.T.; Siminovitch, D.J.; Mantsch, H.H. Structurelarva Chaoborus americanus. J. Insect Physiol. 21:1265–1269;

1975. and properties of model membranes: new knowledge fromhigh pressure vibrational spectroscopy. Biochim. Biophys.45. Thurston, M.H. Scavenging abyssal amphipods from the

North-East Atlantic Ocean. Mar. Biol. 51:55–68;1979. Acta 947:139–171;1988.52. Yayanos, A.A. Recovery and maintenance of live amphipods46. Torsellini, A.; Doni, L.; Palinski, W.; Guidi, G.; Lombardi,

V. Pressure-induced metabolic activation of platelets demon- at a pressure of 580 bars from an ocean depth of 5700m. Sci-ence 200:1056–1059;1978.strated in vitro by determination of malondialdehyde forma-

tion. Thromb. Haemostas. (Stuttgart) 52:4–6;1984. 53. Yayanos, A.A. Reversible inactivation of deep-sea amphipods(Paralicella capresca) by a decompression from 601 bars to at-47. Wardle, C.S.; Tetteh-Lartey, N.A.; Macdonald, A.G.; Harper,

A.A.; Pennec, J.P. The effects of pressure on the lateral swim- mospheric pressure. Comp. Biochem. Physiol. 69A:563–565;1981.ming muscle of the European eel Anguilla anguilla and the deep