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.     

Temperature and pressure tolerance of larvae of Crepidula fornicata suggest thermal limitation of bathymetric range

The extant deep-sea fauna is thought to result from recolonisation of this environment by shallow-water organisms following climate-driven mass extinctions. Planktonic larval tolerance to high pressure is considered an important preadaptation for successful deep-sea invasion. In this study, the pressure and temperature tolerance of a species without any known confamilial deep-sea relative were assessed for the first time. Early- and late-veliger larvae of the shallow-water species Crepidula fornicata were subjected to a temperature/hydrostatic pressure regime from 5 to 25 °C and from 0.1 to 40 MPa. Although early and late veliger survived pressures equivalent to 2,000 m water depth or greater at all temperatures, decreased larval activity indicated significant sublethal temperature and pressure effects. Reduced larval activity of early veliger at low temperatures suggests that the bathymetric range of this species may be thermally constrained. A mechanistic model is proposed to explain the emerging pattern of ontogenetic shifts in pressure tolerance of shallow-water benthic invertebrates.     

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.     

Etude de la respiration chez des copépodes pélagiques méditerranéens (bassin occidental et Mer Ionienne) et de ses variations en fonction de la bathymétrie des espèces et de leur origine géographique

A shipboard experimental study was conducted on the respiratory rate of pelagic copepods from two Mediterranean stations (Ionian Sea and Occidental Basin). In each sampling area, copepods were collected from different depths (0 to 2500 m) by horizontal net hauls. Selected copepod species included bathypelagic, lower mesopelagic, upper mesopelagic and epipelagic species. Respiration rates were determined at 4 different temperatures (10°, 14°, 18°, 22°C). The metabolism-temperature curves revealed varying degrees of thermal sensibility of copepod respiration related to their respective habitats. During experiments employing a large range of temperatures, bathypelagic species proved most sensitive. By contrast, vertically migrating species appeared to be more tolerant to temperature variation. The relationship between respiratory rate and copepod dry weight was investigated for the 4 temperatures used. A strong correlation emerged between log of respiration and log of weight. The equation of regression lines varied with experimental temperature and with geographic origin of the copepods studied. Comparison of the relation respiration-weight of specimens from the two Mediterranean stations and from a previously studied Atlantic station (Canarian and south Moroccan region), indicated that observed differences are related to the average temperature of the mesopelagic waters in each sampling area. The pressure effect on metabolic rate is discussed. It is suggested that hydrostatic pressure does not affect the characteristics of temperature sensibility of copopods' respiration under the temperature conditions prevailing in their natural habitat.     

A dispersal model for larvae of the deep sea red crab Geryon quinquedens based upon behavioral regulation of vertical migration in the hatching stage

Behavioral responses to gravity, hydrostatic pressure, and thermoclines are described for Stage I zoeae of the deep sea red crab Geryon quinquedens Smith. Survival and rate of development as a function of temperature is presented for all larval stages. Although temperatures between 10° and 25°C have no direct effect upon survival, development time is five times longer at 10°C than at 25°C. Stage I larvae show strong negative response to gravity. Swimming rate increases with an increase in pressure up to 20 atm above ambient at 11°C, but not at 15°C. Swimming rates at 15°C are higher than those measured at 11°C at each pressure tested. Stage I larvae readily penetrate sharp thermoclines. Potential dispersal ranges of G. quinquedens larvae in the Mid-Atlantic Bight are suggested based on larval behavior, development time, and coastal hydrography. A testable recruitment model is proposed for G. quinquedens.Contribution no. 1365 of the Center for Environmental and Estuarine Studies     

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.     

Effects of various temperature cycles on the larval development of the gastropod molluscCrepidula fornicata

Veligers ofCrepidula fornicata (L.) were reared for 12 days at constant temperatures of 15°, 20°, 25°, 30° and 35°C, and at 5 C° daily cycles of equal periodicity (COEP) over the temperature ranges 15° to 20°C, 20° to 25°C, 25° to 30°C and 30° to 35°C. COEP consisted of equal periods (6 h) of maximum temperature, minimum temperature, and uniformly increasing and decreasing temperature each 24 h period. Survival was high and not influenced by cyclic or constant temperature from 15° to 30°C. At 35°C and COEP 30° to 35°C, all larvae died before Day 6. Shell growth rate increased markedly over the range 15° to 25°C, and growth rates at cyclic temperatures in this range were intermediate between growth rates at the corresponding constant temperatures. Larvae reared at COEP 15° to 20°C and COEP 30° to 35°C had discontinuities in their shells due to inhibition of shell secretion during the adverse part of each temperature cycle. Groups ofc. fornicata veligers were exposed for 2 days to daily temperature cycles of equal and unequal periodicity in the critical 30° to 35°C range. [Cycles of unequal periodicity (COUP) consisted of unequal periods (varying between 3 and 15 h) of maximum and minimum temperature and uniformly increasing and decreasing temperature each 24 h period.] These veligers showed shell growth although their body tissue declined, as indicated by decreasing carbon content per larva. Least shell growth and most body tissue loss occurred in those cycles with the longest exposure to higher temperature. Larvae exposed for arious days to the mildest 30° to 35°C COUP (15 h at 30°C, 3 h increasing temperature, 3 h at 35°C and 3 h decreasing temperature) recovered and resumed normal growth when transferred to constant 30°C, but their growth was retarded in proportion to the number of days in the temperature cycle. Rates of shell growth of veligers in temperature cycles show an immediate effect of environmental temperature, while changes in carbon content per larva better reflect the effects of temperature on general metabolism and survival.     

Der einfluß der temperatur auf thermostabilität,isoenzym-muster und reaktionskinetik der laktat-dehydrogenase aus fischen

Methodological problems complicate investigations on thermostability of lactate dehydrogenase (LDH). It is difficult to demonstrate a correlation between adaptation-temperature (AT) and LDH thermostability. Heat-inactivation characteristics change completely if diluted or undiluted tissue extracts are heated. In purified LDH (purchased from Boehringer, Mannheim, FRG), additions such as casein, bovine-serum albumin, NADH and pyruvate — even in small concentrations — can alter considerably the degree of heat resistance. It LDH activity is measured as a function of experimental temperature (ET) according to the composition of the actual test mixture (e.g. altered pyruvate concentration), a different temperature optimum is found. If tissue extracts containing unpurified enzymes are used, the accompanying substances act on the enzyme and modify its properties. Thus, possible influence of AT on enzyme properties can be concealed (suppressed, over-emphasized). In Idus idus acclimated to 10° or 20°C, brain, gill, gut and white dorsal muscle reveal identical LDH-isoenzyme patterns. However, liver-LDH shows a pattern dependent on the AT. A total of 11 bands with LDH activity were found. In 10°C fishes, the Isoenzymes 1, 3, 6 and 7 are especially active. However, 20°C fishes show marked activity of Isoenzymes 5 and 8, and a reduced activity of Isoenzyme 7. According to their electrophoretic mobility, the particular isoenzymes of LDH of white dorsal muscle of I. idus or Rhodeus amarus can be clearly distinguished. The ATs 10° or 20°C do not influence the dependence of reaction order on ET: this is not true for the velocity constant.     

Respiration and chemical composition of the bathypelagic euphausiid Bentheuphausia amblyops

Bentheuphausia amblyops is a cosmopolitan bathypelagic euphausiid with a vertical range of from 280 to 7 000 m. Determinations of proximate and elemental composition show that B. amblyops has a more robust structure (lower water content and higher protein content) than is typical of other bathypelagic Crustacea. B. amblyops is a strong swimmer and is capable of employing its thoracic legs in raptorial fashion. Discrete depth trawls taken between depths of 400 and 2 500 m on a diel basis show no evidence of vertical migration. There was no significant difference in oxygen consumption within the species environmental temperature range (1.5° to 7.5°C), which may be partially ascribed to a limited temperature effect and partially to variability in spontaneous activity at the different temperatures. Between 7.5° and 9.5°C there was a marked temperature effect on metabolism (Q₁₀=6.4). The observed vertical distribution and metabolic response to elevated temperature preclude the migrations to the surface that have been postulated for B. amblyops. The robust composition of the species, its behavioral characteristics, and published diet information strongly suggest that the species is omnivorous with a strong predatory component in its foraging strategy.     

Effects of constant and cyclic temperatures on the salinity tolerance of the estuarine sandhopper Orchestia chiliensis

The survival of Orchestia chiliensis (Milne Edwards, 1840) was investigated at salinities between 0.3 and 68 and constant or 10 C° cyclic temperatures between 5° and 25° C. Mortality increased with age, temperature and at salinity extremes. Small individuals show little seasonal acclimatisation apart from increased thermal tolerance at the highest exposure temperature. Larger individuals show a lateral shift in the mortality curve to the right in summer, giving increased survival at most salinities. Salinity had less effect on amphipods in cyclic regimes and survival was similar in 5° to 15° C and 10° to 20° C cycles. Mortality of larger individuals was higher in the 15° to 25° C cycle, but seasonal acclimatisation gave increased resistance at all fluctuating temperatures during the summer. Mortality in cyclic temperatures was higher than at similar constant temperatures. O. chiliensis does not actively evade immersion and diel temperature changes of 10 C° represent an important stress factor. This would affect all life stages and influence field populations both in the winter and the summer.     

Method for indirectly defining optimum temperatures of inhabitancy for marine cold-blooded animals

Investigations on the influence of pressure on the activity of alkaline phosphatase of some marine invertebrates from the Baltic Sea were carried out at temperatures between 5° and 55°C. The results obtained indicate that the influence of pressure on alkaline phosphatase activity is modified by temperature. At low temperatures, pressure has a decreasing effect on enzyme activity, while it has an increasing effect at higher temperatures. The gill homogenates of the relatively pressure-resistent bivalves Cyprina islandica and Mytilus edulis show a lower decrease of activity under pressure at low temperatures than the gill-homogenate of Carcinus maenas and a purified enzyme preparation of a homoiothermal animal.     

Effect of temperature on permeability and drinking rates of the metanauplii of the brine shrimp Artemia sp.

Diffusional permeabilities and drinking rates of 24 h-old Artemia sp. metanauplii incubated at 20 °C were studied at five temperatures: 15, 20, 25, 30, and 35 °C over a period of 6 h. Departures from the incubation temperature resulted in changes in both permeability and drinking rates which both reached their highest values at 35 °C. Metanaupliar permeability and drinking were more elevated than previously reported for adults.     

Comparative studies on the metabolism of shallow-water and deep-sea marine fishes. V. Effects of temperature and hydrostatic pressure on oxygen consumption in the mesopelagic zoarcid Melanostigma pammelas

Measurements have been made of routine oxygen consumption rates ( ) of the mesopelagic deep-sea zoarcid fish Melanostigma pammelas. Determinations were made over ecologically relevant ranges of 3 variables; temperature (3° to 10°C), hydrostatic pressure (1 to 170 atm), and oxygen partial pressure (1 to 160 mm Hg). Weight-specific s were uniformly low. Of the 3 test variables, only temperature had significant metabolic effects within the ranges studied. Q₁₀'s were 6.75 between 3° and 5°C. 1.47 between 5° and 7°C, and 17.4 between 7° and 10°C. These Q₁₀'s were constant over the hydrostatic pressure range studied. Between 3° and 7°C the fish regulated their rates of oxygen consumption down to PO₂'s comparable to those occurring in their natural environments (6 to 12 mm Hg). The showed no capacity to tolerate anoxic conditions. The physiological and ecological significance of these results is discussed, particularly with reference to thermal effects and to the basis of survival of this fish in the oxygen minimum layers of the eastern Pacific Ocean. Since it is possible to maintain M. pammelas in the laboratory for extended periods of time (over 12 months) it could serve as the basis for many interesting studies of deep-sea fish biology.     

Metabolic adaptation of Cancer irroratus developmental stages to cyclic temperatures

Metabolic-temperature responses of the developmental stages of the sublittoral crab Cancer irroratus cultured at 10° to 20°C daily cyclic and 15°C constant temperatures were determined. Generally, the metabolic rate increased with temperature in the lower range with Q₁₀'s (temperature coefficients) above 2, compensated in the midrange with Q₁₀'s between 1 and 2, and declined at the higher temperatures with Q₁₀ values less than 1. For the larvae cultured at a constant temperature of 15°C, the compensatory response range narrowed with development from first zoeae to the later zoeal stages. In contrast, the compensatory response of the first zoeae, megalops, and crab stages within the range 10° to 25°C was interrupted by a zone of thermal sensitivity between 15° and 20°C for those individuals cultured in the 10° to 20°C cyclic regime. The compensatory response range is narrower for the third stage zoeae and broader for the second, fourth, and fifth stage zoeae. Metabolic rate-temperature (M-T) patterns of C. irroratus developmental stages cultured under the cyclic regime varied from those held at constant temperature by increased respiration and metabolic rate compensation between 20° and 25°C, and by an extension of the metabolically active range towards higher temperatures.     

Effects of nutrition and temperature on metabolic enzyme activities in larval and juvenile red drum,Sciaenops ocellatus,and lane snapper,Lutjanus synagris

The metabolic enzyme activities were determined in larvae of red drum, Sciaenops ocellatus, and lane snapper, Lutjanus synagris, to determine the effect of temperature and nutrition on metabolic enzyme activities and to evaluate if metabolic enzyme activities are useful in assessing the feeding condition of larval fish. During experiments conducted during the spring of 1990, lactate dehydrogenase (LDH) activities in both red drum and lane snapper were approximately an order of magnitude lower than values typical for adult fish; LDH and citrate synthase (CS) activities increased during early developmental stages, but nutritional effects were apparent. Clear differences (up to 4-fold) between well-fed and starving fish were evident in both LDH and CS activity in red drum. Differences between well-fed and poorly fed larvae were evident until 9 d after hatching. Lane snapper larvae reared at a 25°C had significantly lower LDH activities than larvae reared at 28°C.     

Comparative thermal metabolic patterns in Euterpina acutifrons dimorphic males

Thermal metabolic acclimation patterns have been determined for cold-and warm-acclimated dimorphic males of the copepod Euterpina acutifrons. The copepods were acclimated either to 15° or 25°C. Metabolic measurements were made at the two acclimation temperatures. At 25 °C, the small males had a higher rate than the large ones. At 15 °C, the large males had the higher rate. The metabolic pattern of thermal acclimation is also distinctive in the two forms. Small males showed metabolic adaptation at the lower acclimation temperature (15 °C), but not at the higher acclimation temperature (25 °C). In the large males the acclimation patterns were reversed, i. e., these males acclimated at the higher temperature, not at the lower. The acclimation patterns based on Precht's (1958) scheme of acclimation are entirely different in the two forms.Supported by PHS grant 5-SO5-FR-07070-02.     

The effect of temperature and thermal distribution on glycolysis in two rockfish species (Sebastes)

Studies on the effects of temperature on the activities of Embden-Meyerhof (EM) glycolysis, and the hexose monophosphate shunt (HMP) in fishes have dealt mainly with exotic and/or acclimated fishes. This study reports the effects of short-term reductions in temperature on EM and HMP activity in two closely related species of temperate fishes (Sebastes spp.) and its possible relation to the thermal distribution of the species. Thermal distribution data were collected by SCUBA for S. mystinus and S. serranoides in King Harbor, Redondo Beach, California, USA. Activities of the pathways were determined in liver-tissue studies, using glucose-¹⁴C and liquid scintillation techniques following the method of Hochachka (1968) with modifications. The data were analyzed by distribution-free methods. Tissue studies indicated HMP activity in both species at lowered temperature (5°C), but only in S. serranoides at 15°C. Results indicate that S. mystinus is capable of instantaneous temperature compensation, possibly related to its tendency to occupy cold waters.     

Metabolism,enzymic activities and cold adaptation in Antarctic mesopelagic fishes

Several species of Antarctic mesopelagic fishes that have different minimal depths of occurrence but the same environmental temperature were collected in November–December 1983 and in March 1986 between 0 and 1 000 m in the open water near the marginal ice zone in the vicinity of 60°S 40°W (1983) and 65°S 46°W (1986), and oxygen consumption rate (V _{O 2}) and the activity of two metabolic enzymes, lactate dehydrogenase (LDH, an indicator of the anaerobic potential of locomotory muscle) and citrate synthase (CS, an indicator of citric acid cycle activity or aerobic potential), were determined. In four dominant species, whole-individual oxygen-consumption rate (y, ml O₂ individual^–1 h^–1) varied with weight (X, g) according to the equation y=aX ^b, with b values falling between 0.889 and 1.029. The relation of weight-specific LDH activity (y, U g^–1 wet wt) with weight (x, g) was also described by the equation y=aX ^b, with b values varying between 0.229 and 1.025. Weight-specific CS activity declined with weight, with b values from-0.031 to-0.369. V _{2 O}, LDH activity and CS activity all declined markedly with increased species' minimum depth of occurrence (the depth below which 90% of a species' population lives). Comparisons with previous studies on ecologically equivalent species of the California Borderland indicate that depth-related decreases in metabolism are the result of adapted traits of deeper-living species, not declining temperature within the water column. The metabolic rate of Antarctic mesopelagic fishes is approximately twice that of California species at equivalent temperatures; similar rates were found at the normal habitat temperatures of the two groups. Thus, a well-developed compensation for temperature is present in the Antarctic fishes: cold adaptation. Differences in enzymic activity among species, and among different sized individuals of a species are related to differences in metabolic rate and locomotory capacity. Enzymic indices can be used to estimate metabolic rates and evaluate ecological parameters such as predatory strategies and niche separation.     

NADP+-isocitrat-dehydrogenase aus Idus idus (Pisces: Cyprinidae). I. Aktivität als funktion der adaptationstemperatur

Activity of NADP⁺-dependent isocitrate dehydrogenase (ICDH) of the white dorsal muscle of Idus idus L. was determined by special analysis, under optimum homogenisation, centrifugation and cuvette conditions. The experimental conditions differed considerably from those used for the investigation of NADP⁺-ICDH activity in mammals by Bücher et al. (1964). Daily measurements of activity over a period of 10 days revealed variations in enzyme activity which are difficult to explain. However, the variations are smaller than those established in earlier tests. In order to obtain statistically valid results, the highest possible number of test fishes (at least 10 individuals for each measurement) must be investigated over a period of 5 to 10 days. NADP⁺-ICDH of individuals acclimated to 10°C showed 28% higher specific and non-specific activity than that of fish maintained at 20°C (experimental temperature 25°C). At 5 different adaptation temperatures, increasing activities were observed with decreasing adaptation temperature (compensation). These measurements were made over a period of 5 successive days.     

Some effects of temperature on the growth and metabolic rate of juvenile blue crabs,Callinectes sapidus,in the laboratory

Juvenile blue crabs, Callinectes sapidus Rathbun, were grown in the laboratory at different temperatures, and metabolic-rate determinations were made. Growth is shown to be dependent upon temperature. Crabs kept at high temperatures (34° and 27°C) grow faster than those kept at lower temperatures (13°, 15°, and 20°C). Increase in size per molt is less at higher temperatures than at lower ones. Mortality is directly proportional to temperature between 13° and 34°C and is very high during ecdysis at elevated temperatures. Metabolic rate increases with temperature, but various degrees of acclimation are seen after 4 weeks exposure. No acclimation of general activity to temperature was found. The findings are applied theoretically to crabs living in the region of heated discharge canals of electrical generators: the motile blue crab could extend its growing season without decreasing size at maturity by active selection of thermal surroundings.In part based on a thesis submitted in partial fulfillment of the requirements for the Degree of Master of Science at the University of Florida, USA.