Comparative studies on the metabolism of shallow-water and deep-sea marine fishes. I. White-muscle metabolism in shallow-water fishes

Maximal rates of oxygen consumption in vitro have been measured under standardized conditions at three test temperatures (5°, 15°, and 25°C) on minced preparations of white muscle from 39 species of shallow-water marine teleost fishes. These fishes came from four different geographic areas, two with cool average water-temperatures (near 15°C: coastal southern California, Galápagos Islands) and two with warm average water-temperatures (near 25°C: Hawaiian Islands; Bermuda). The group includes species covering much of the range of variation to be found among the teleosts with respect to five additional variables: phylogenetic position, type of environment, body weight, activity level, and growth stage. The purpose of the work is to provide part of a base line of tissue-metabolism data on shallow-water fishes for comparison with similar results from deep-sea species. Major conclusions from statistical analyses of the results are: four groups of shapes of oxygen-uptake rate versus temperature curves exist: normal, flat, dipped and peaked. Over 50% of curves are normal. Intra-group differences, contributing significantly to the total variance of the results at given test temperatures, are: cool versus warm average environmental temperatures primarily for epipelagic species; epipelagic versus non-epipelagic environments; very active species versus all others; juvenile stages versus adults. In each case, the subgroup first mentioned shows higher muscle oxygen-uptake rates than the other subgroup. Variables not contributing significantly to the total variance are phylogenetic position and body weight. Physiological and ecological implications of these results are discussed.     

Comparative studies on the metabolism of shallow-water and deep-sea marine fishes. II. Red-muscle metabolism in shallow-water fishes

Maximal rates of oxygen consumption in vitro have been measured under standardized conditions at three test temperatures (5°, 15°, 25°C) on minced preparations of red muscle from 10 species of shallow-water marine teleost fishes. These fishes came from three different geographic areas, two with cool average water temperatures (near 15°C: coastal southern California, Galápagos Islands) and one with warm average water temperatures (near 25°C: Hawaiian Islands). The group is made up of post-juvenile or adult epipelagic fishes, which are moderately or very active in terms of their locomotor activities. A large part of the range of phylogenetic diversity among the teleosts is represented, as is the body weight range from a few grams to several kilograms. The purpose of the work is to provide part of a set of tissue-metabolism data on shallow-water fishes for future comparison with similar results from deep-sea species. Of 8 complete curves for oxygen uptake rate versus temperature (R-T curves), 6 are normal in shape (Q₁₀1.5), 1 is normal but with a low Q₁₀, and 1 is partly flat, partly normal. The differences between the species in terms of both absolute positions and slopes of the R-T curves are not related in any consistent way to any of the three testable variables: phylogenetic position, long-term adaptation temperature, and body size. The red muscles of a variety of adult epipelagic fishes, at ecologically realistic temperatures, are shown to be exceptions to the general rule that tissues of ectothermous lower vertebrates have lower metabolic rates than comparable tissues of non-torpid endothermous higher vertebrates. This circumstance probably is a major factor in the great capacities for sustained high-speed swimming shown by most epipelagic fishes. Other physiological and ecological implications of the results are discussed.     

Comparative studies on the metabolism of shallow-water and deep-sea marine fishes. IV. Patterns of aerobic metabolism in the mesopelagic deep-sea fangtooth fish Anoplogaster cornuta

Measurements have been made of oxygen consumption rates O₂ of 10 specimens of the mesopelagic deep-sea fangtooth fish Anoplogaster cornuta. Determinations were made at 1 atm pressure, at temperatures of 3°, 7°, and 10°C, at dissolved oxygen concentrations ranging from near saturation to zero, with the fish swimming at low, controlled speeds. Weight-specific O₂ were uniformly low. They showed Q₁₀'s of 2.5 and 1.3, respectively, in the temperature ranges 3° to 7°C, and 7° to 10°C, at dissolved oxygen concentrations above 2 ml (standard temperature and presusure, STP)/1. Measurable O₂ continued in these fish at dissolved oxygen concentrations down to the lowest levels detectable with our instruments. At 7°C the average critical oxygen tension (P _c ) for the entire group was near 35 mm Hg. However, there is a statistically significant positive slope to the regression line relating O₂ to P _c for individual fish. The physiological and ecological significance of these results is discussed, particularly with reference to thermal effects and to the basis for survival by A. cornuta in the oxygen minimum layers of the eastern Pacific Ocean.     

Comparative studies on the metabolism of shallow-water and deep-sea marine fishes. III. Apparatus for studies of tissue preparations under high hydrostatic pressures

Design information is given for hydrostatic-pressure apparatus permitting either intermittent or continuous monitoring of the rates of nonoptically observable biochemical and physiological processes in the fluids supporting surviving preparations of living tissues or tissue fractions. Semi-micro scale experiments can be carried out over the full range of temperatures and hydrostatic pressures occurring in the oceans of the world. Samples are obtained at 1 atm pressure, whatever the experimental pressure. The apparatus is simple to use, safe, reliable, and readily portable for work on shipboard. Specially designed components described in detail are: magnetically stirred pressure vessels, sampling valves, and magnetic stirrer drive.     

The effect of pressure on muscle lactate dehydrogenase activity of some deep-sea and shallow-water fishes

The activity of crude muscle lactate dehydrogenase (LDH) of several species of bathypelagic and shallow-water fishes has been measured at pressures between 1 and 578 atm and at temperatures of 15° and 25°C. No relationship has been found between the effect of pressure on enzyme activity and the hydrostatic pressure of the organism's environment. Applied hydrostatic pressure reduced activity at both temperatures. The decrease at 25°C was double the decrease at 15°C in LDH from shallow-water fishes. However, enzymes from 2 bathypelagic fishes showed approximately the same reduction at both temperatures. Thus, the interaction of temperature and pressure was less in deep-sea than in shallow-water fish LDH. Decreasing temperature and increasing pressure would both reduce the activity of LDH. That is, deep-sea conditions are noncompensatory in this instance. It is possible that the dissociation of the effects of temperature and pressure could be an adaptive feature of deep-sea life.This paper is a portion of a thesis submitted to the Graduate School, University of Georgia, in partial fulfillment for the degree of Master of Science.     

Interacting pressure and temperature effects on enzymes of marine poikilotherms: Catalytic and regulatory properties of FDPase from deep and shallow-water fishes

At low temperature (3°C), and in the absence of substrate and cofactor, the enzyme, fructose diphosphatase (FDPase), extracted from liver of the benthic fishCoryphaenoides acrolepis, is reversibly inactivated by exposure to relatively low pressures (5,000 psi). At pressures of 20,000 psi at 3°C the native enzyme is irreversibly denatured. When the cofactor and the substrate are present, the enzyme is protected against pressure denaturation; hence, catalysis is insensitive to at least 10,000 psi at 3°C. Similarly, interactions between FDPase and its negative modulator adenosine monophosphate (AMP), are largely pressure insensitive. Pressure sensitivity of the native enzyme and of the catalytic process is much reduced at temperatures above about 9°C. The homologous enzyme from a surface fish,Pimelometopon pulchrum, is strikingly more sensitive to pressure, particularly at low temperatures.     

Effects of pressure,temperature and oxygen on the oxygen consumption rate of the Midwater copepod Gaussia princeps

In this study we assessed the amount of lead accumulated in the body of a grazing mollusc by transfer from its algal food in laboratory experiments, and compared these results with the amounts found in naturally occurring molluscs and seaweed. Near La Jolla, California (USA), where the concentration of lead in seawater is probably less than 0.08 g l^-1, most of the naturally occurring Egregia laevigata contains less than 0.4 g Pb g^-1 wet weight. The total body masses, without shells, of juvenile Haliotis rufescens fed on this seaweed for 3 to 6 months showed similar concentrations. When, however, E. laevigata is placed for 1 to 6 days in seawater to which lead has been added (0.1 or 1.0 mg l^-1) both the seaweed and the abalone subsequently fed with it accumulate proportionally larger amounts of lead. After 6 months, young abalone fed on E. laevigata pretreated with 1.0 mg Pb l^-1 accumulated up to 21 g Pb g^-1 wet weight. This amount of lead had no apparent consequences on the growth or activity of the molluscs. Analyses of 6 different organs from adult abalone showed that the lead was selectively concentrated in the digestive gland. In the foot (muscle tissue), which is the part normally consumed by humans, only negligible amounts were found.     

The effects of temperature and pressure acclimation on the temperature and pressure tolerance of the shallow-water shrimp Palaemonetes varians

Anthropogenic effects on marine ecosystems (e.g. hypoxia, warming) at and beyond continental margins are assumed to affect physiological and biochemical boundaries to species’ distributions, potentially leading to habitat contraction across depth. Whether or not shallow-water benthic invertebrates are capable of undergoing depth-related migrations in response to such perturbations remains largely unknown. The few studies available have focused solely on whether colonisation of deep waters may be ongoing and on the ability of shallow-water species to tolerate low temperatures and high hydrostatic pressures: two physical parameters, which are thought to limit the depth range of a species. Those studies did not consider the effects of acclimation to low temperature and, especially, acclimation to high hydrostatic pressure on pressure tolerance. We demonstrate that acclimation to both low temperature (5 °C) and to high hydrostatic pressure (10 MPa) increases the pressure tolerance within the shallow-water shrimp Palaemonetes varians. Previous studies have demonstrated the impressive temperature and pressure tolerance of this shallow-water shrimp. Here, we provide evidence that a shallow-water species may acclimate to low temperature and high pressure and show greater pressure tolerance, suggesting that shallow-water organisms may be able to rapidly—and potentially stepwise—acclimate to the low temperature and high pressure conditions typical of the deep sea. These findings are of importance for understanding phylogenetic development from shallow- to deep-water species and the processes behind past, present and future bathymetric range shifts in species.     

Scavenging deep-sea amphipods: Effects of food odor on oxygen consumption and a proposed metabolic strategy

In situ respiration rates as a response to the odor of food were measured for two species of scavenging amphipods, Paralicella caperesca from 3 650 m in the western North Atlantic Ocean and Orchomene sp. B from 1 300 m in the Santa Catalina Basin off southern California (USA). In addition, complementary laboratory starvation/respiration rates for a shallow-water species, Orchomene sp. A, were determined. Initial elevated O₂ consumption rates were found for up to 8 h in all deep-sea amphipods exposed to bait odor, followed by a period of lowered respiration equivalent to rates observed in individuals not exposed to bait. Orchomene sp. A revealed a response similar to that observed in the deep-sea species. A metabolic strategy is proposed whereby scavenging amphipods efficiently utilize large episodic organic falls in the food-limited environment of the deep sea. This strategy involves (1) the ability to withstand long periods of starvation, (2) rapid response to an organic fall, (3) rapid location of the organic fall, (4) maximal rate of food consumption with maximal quantity ingested, and (5) efficient utilization of the consumed food. Each of these attributes are explored with the expected and observed mechanisms employed to achieve them.     

Patterns and selectivity in the feeding of certain mesopelagic fishes

Stomach contents were analysed from the 7 most numerous species of mesopelagic fish caught in a series of 11 hauls over a 24 h period at 230 to 266 m depth in the eastern North Atlantic Ocean. The numerical abundance of organisms per filled stomach and the frequency of occurrence of empty stomachs were used to indicate feeding periodicity. The ecological significance of the feeding periodicity was considered by examining it in connection with an investigation of the day-night vertical distribution of zooplankton and micronekton to 2000 m at the same station. Additional dietary evidence on the 7 species considered was also obtained from the vertical series. Feeding selectivity was examined by comparing the composition of the zooplankton population, sampled separately but simultaneously with the micronekton, with that from the overall stomach contents of the species examined. Feeding periodicity was demonstrated for 6 species, of which 3 were found to be feeding selectively: Valenciennellus tripunctulatus on calanoid copepods, Argyropelecus aculeatus on ostracods, and Lampanyctus cuprarius on amphipods and possibly euphausiids. The limited data available on the other 3 species suggested that they were either random feeders (A. hemigymnus and Lobianchia dofleini) or perhaps selecting against a particular group (Notolychnus valdiviae). No indication of feeding periodicity or selectivity was found for Chauliodus danae. The overall pattern of results confirmed the supposed close correlation between vertical migration and feeding in mesopelagic fish.     

Effects of environmental parameters on the oxygen consumption of four marine invertebrates: a comparative factorial study

The oxygen consumption curves of two decapod crustaceans (Palaemon serratus, Penaeus monodon) and two prosobranch molluscs (Trunculariopsis trunculus, Nassarius mutabilis) have been detected in the entire pO₂ interval from 0 to 160 mmHg, under different conditions of temperature and salinity. From the experimental curves, physiological parameters such as the initial oxygen consumption velocity, the Q ₁₀ values and the oxygen independence indices have been measured. The latter parameters have been obtained using normalised plots which allow their better evaluation. The effects of temperature, salinity and oxygen partial pressure on the oxygen-consumption features have been studied using a factorial experimental plan which allows measurement of the effects of each experimental variable as well as the effects of synergistic interactions between different variables. Received: 27 March 2000 / Accepted: 13 November 2000     

Temperature effects on behavior and survival of marine invertebrates exposed to variations in hydrostatic pressure

Investigation into the pressure resistance of 8 intertidal species belonging to the genera, Uca, Sesurma, Talorchestia and Littorina from the Northern Gulf of Mexico and Panama sheds light on the relationships between temperature and hydrostatic-pressure resistance. Generally, increasing temperature increases the pressure required to elicit reversible reactions such as increased activity and tetany, or paralysis, wheroas increasing temperature generally evokes the irreversible response of death (LD₅₀) at a decreasing pressure. Tropical stenotherms tend to be more sensitive to hydrostatic pressure than eurythermal-temperate species at the same or similar temperatures.     

Effects of temperature and delayed feeding on growth and survival of larvae of three species of subtropical marine fishes

In larvae of the bay anchovy Anchoa mitchilli (Valenciennes), the sea bream Archosargus rhomboidalis (Linnaeus), and the lined sole Achirus lineatus (Linnaeus), growth, survival, and starvation times were investigated at temperatures of 22° to 32°C. The rate at which hours after hatching until starvation decreased in relation to temperature for unfed larvae did not differ significantly among the 3 species, ranging from-5.4 to-6.3 h per degree increase in temperature. The total number of hours until starvation did differ for all 3 species: lined soles survived longest, bay anchovies were intermediate, and sea bream survived the least time. At 28°C, unfed sea bream could survive 90.1 h, bay anchovy 102.3 h, and lined sole 119.8 h. The eyes pigmented at nearly the same time after hatching for sea bream and bay anchovy, but took about 20 h longer at all temperatures for lined sole. Quadratic equations best described the relationship between hours after hatching when the eyes became pigmented and temperature. Eye-pigmentation times became nearly constant for all 3 species at temperatures above 28°C. At 28°C, eyes pigmented about 27 h after hatching for bay anchovy and sea bream but not until 47 h for lined sole. Hours after eye pigmentation when unfed larvae starved was a measure of the effective time that larvae had to commence feeding. Bay anchovies and lined soles were nearly alike in this respect, but sea bream starved at tewer hours after eye pigmentation. Slopes of regressions representing decrease in times to staration for increasing temperatures ranged from-3.7 to-4.4 h per degree increase in temperature, and were not significantly different among the 3 species. At 28°C, unfed lined soles starved at 70 a after eye pigmentation, bay anchovies starved at 72.5 h, and sea bream at only 62 h. Yolk absorption was most rapid for all species during the first 20 h after hatching, and was faster at higher temperatures. Amounts of yolk remaining at the time eyes became pigmented were less at higher temperatures for bay anchovy and lined sole, but were greater for sea bream, suggesting that sea bream used yolk more efficiently at higher temperatures. Either no yolk or small traces (>0.20%) remained at 24 h after eye pigmentation in all 3 species. Feeding was delayed for periods of 8, 16, 24, 32, 40 and 48 h after eye pigmentation for all species at a series of experimental temperatures from 24° to 32°C. Growth and survival were affected when food was withheld for more than 24 h at 28°C, but survival did not decrease markedly until food was withheld at least 8 h longer. At lower temperatures food could be withheld longer and at higher temperatures for less time. Feeding can be initiated by most larvae for several hours after all visible yolk reserves have been exhausted. All species tested can survive for 24 to 40 h after eye pigmentation at 24° to 28°C without food and still have relatively good growth and survival when food is offered. If the “critical period” is considered relative to time of hatching, lined soles need not find food for 3 to 3.5 days after hatching, but bay anchovy and sea bream must feed within 2.5 days of hatching.     

Effects of temperature,seawater osmolality and season on oxygen consumption and osmoregulation of the amphipod Gammarus oceanicus

Seasonal variations of oxygen consumption rate, haemolymph osmolality and the concentrations of the inorganic ions potassium and sodium in the haemolymph were measured in the littoral amphipod Gammarus oceanicus collected from the Trondheimsfjorden, Norway in 1987. For each season comparisons were made of amphipods acclimated for 1 wk to 0.5, 4.5, 10.0, 15.0 and 20.0°C, in combination with seawater osmolalities of 100, 500 and 1200 mOsm and to the seawater osmolality corresponding to that of the collecting site. The oxygen consumption rate showed a temperature insensitivity when the amphipods were acclimated to low temperatures in winter and high temperatures in summer. Significant differences were found in oxygen consumption between individuals acclimated to various medium osmolalities, possibly indicating higher energy requirements for osmotic and ionic regulation at low seawater osmolalities. Oxygen consumption rate was significantly higher in summer than in other seasons. Haemolymph osmolality and the concentration of the inorganic ions sodium and potassium were not influenced by temperature or season. Determination of haemolymph osmolalities and concentrations of inorganic ions revealed that G. oceanicus is a strong hyper-osmotic and hyper-ionic regulator in dilute seawater. The concentration of potassium in the haemolymph is less influenced by seawater osmolality than haemolymph osmolality and the haemolymph concentration of sodium.     

Comparative study of the effects of temperature,salinity and oxygen tension on the rates of oxygen consumption of nauplii of different strains of Artemia

The effects of temperature, salinity and oxygen tension on the rates of oxygen consumption of three different strains of Artemia nauplii have been studied. When acclimated to a salinity of 30, nauplii from each of the three strains were able to maintain approximately constant rates of oxygen consumption over a wide range of oxygen tension. The ability to maintain respiratory independence during hypoxia was reduced, however, with an increase in either temperature or salinity. Nauplii of two of the strains (parthenogenetic diploid and tetraploid) showed a progressive increase in the rate of oxygen consumption with increasing temperature up to 35°C. Nauplii of the bisexual strain appeared to be less tolerant of exposure to temperatures >30°C, since at higher temperatures their oxygen consumption declined slightly. The differences between the nauplii of the different strains in their physiological responses to changing environmental conditions appear to correlate well with their seasonal occurrence in the field.     

Effect of hydrostatic pressure and temperature on the activity and synthesis of chitinases of Antarctic Ocean bacteria

The formation of chitinases by psychrophilic and psychrotrophic marine Antarctic bacteria and the activity of these extracellular enzymes were investigated under simulated deep-sea conditions. The formation of the chitinases was affected by hydrostatic pressure of 400 bars. However, the extent of pressure inhibition differed with the bacterial strains tested and was considerably less with the extreme psychrophilic bacteria isolated from sediments of greater depth. Growth of these psychrophilic strains had a moderately barophilic character at 400 bars, whereas growth of the psychrotrophic strains was clearly restricted under simulated deep-sea conditions. With regard to the activity of the extracellular chitinases of various bacterial strains, a relatively uniform response was found. All chitinases were highly barotolerant at near neutral pH and were active up to 1000 bars. Low temperatures reduced their activity but not their barotolerance. A low pH of 5.1 diminished the barotolerance of some chitinases. The results suggest that the indigenous deep-sea bacteria are capable of decomposing chitin settled to or produced in the depth of the Antarctic Ocean.     

Interaction of temperature and salinity on oxygen consumption of the estuarine crab Panopeus herbstii

Marine Biology - The combined effects of temperature and salinity on the rate of oxygen consuption by the estuarine crab Panopeus herbstii Milne-Edwards (Crustacea: Decapoda: Xanthidae) were...     

Effects of mercury on the behaviour and oxygen consumption of Monodonta articulata

The trochid snail Monodonta articulata Lamarck was exposed to mercuric sulphate at concentrations of 0.2, 0.5, 0.8 and 1 ppm Hg⁺⁺. At 24 h, retraction into the shell was observed in 0.8 and 1 ppm Hg⁺⁺; this retraction increased in these concentrations at 36 h. Retracted snails died if retained in the solutions, but generally recovered within 24 to 48 h if transferred to uncontaminated sea water. Immersionemersion behaviour and interface activity were studied over 24 h by means of an aktograph; snails in normal sea water spent more time below than above the water surface, and exhibited frequent periods of activity. Exposure to mercuric sulphate at concentration of 0.25, 0.5, 0.8 and 1 ppm Hg⁺⁺ progressively reduced both the length and frequency of activity periods. From 0.5 ppm Hg⁺⁺ upwards, emersion periods increased, and immersion periods decreased. Oxygen consumption of snails was measured in sea water and in mercuric sulphate at concentrations of 0.2, 0.5, 0.8 and 1 ppm Hg⁺⁺. Oxygen consumption decreased significantly with each progressive rise in mercury concentration. It is considered that mercury affects M. articulata by interfering with respiration, initially reducing interface activity, then forcing the snail for longer and longer periods out of the water. Retraction occurs when activity is no longer possible. It is concluded that respiratory and behavioural alterations of this nature would afford a good indicator of the presence of sub-lethal concentrations of pollutants.     

Cadmium accumulation,LC50 and oxygen consumption in the tropical marine amphipod Elasmopus rapax

Adult Elasmopus rapax, collected from the eastern coast of Venezuela in 1990, were exposed to seawater containing various CdCl₂ concentrations ranging from 0.25 to 5.5 mol l^-1. The 48-h and 96-h LC₅₀ values obtained were 4.0 and 1.6 mol Cd l^-1, respectively. In amphipods exposed to 1 mol Cd l^-1 for up to 240 h, the apparent rate of cadmium uptake was higher in dead animals (most of which had molted during the preceding 24 to 48 h) than in those which survived throughout the treatments without molting. Thus, whole-body cadmium content reached 1.74 mol g^-1 dry weight (dw) in the former and only 0.85 mol g^-1 dw in the latter; the higher body Cd-load may have caused the increased mortality observed in molters. On exposure to cadmium levels above 0.5 mol l^-1 the oxygen consumption rate of non-molters decreased from 2.2 to about 1.5 ml O₂ g^-1 dw h^-1 over the first 24 h, remaining unchanged thereafter. The results place E. rapax among the most sensitive marine organisms yet studied concerning cadmium toxicity, and emphasize the usefulness of the Amphipoda as bioindicators and research tools for bioassays.     

Influence of salinity and temperature on the oxygen consumption in young juveniles of the Indian prawn Penaeus indicus

Routine oxygen consumption of very young juveniles (0.1 g) of Penaeus indicus H. Milne Edwards was significantly influenced by ambient temperature and weight of the animal, but not by ambient salinity, when tested at salinities (7, 21, and 35) to which they had been long-term (over 10 days) acclimated. Standard oxygen consumption of young juvenile prawns (1 to 3 g), subjected to step-wise changes in ambient salinity, from sea water to low salinity waters (2 to 6), and measured after short-term (24 h) salinity acclimation at each step, was lowest at salinities where prawns such as those tested occur naturally (10 to 15). The metabolic rates do not appear to have a direct relation to the osmotic gradient, even when the influence of interfering activity is eliminated. It appears that factors other than osmotic gradient will have to be sought in order to explain the metabolic patterns of P. indicus in relation to salinity.