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.     

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.     

Sulfide tolerance and detoxification in shallow-water marine fishes

Hydrogen sulfide is a potent inhibitor of aerobic respiration. Sulfide is produced in sediments, and many species of fish live in association with the bottom. Tolerance tests, enzyme assays, and chromatography of sulfur compounds in thirteen species of shallow-water marine fishes (collected in San Diego, California, USA in 1987–1988) indicate adaptations to sulfide that vary with habitat and lifestyle. Tidal-marsh inhabitants, like Gillichthys mirabilis and Fundulus parvipinnis, have higher tolerance to sulfide (96 h LC₅₀ at 525 to 700 M) relative to outer-bay and open-coast inhabitants (surviving <12 h at much lower concentrations). The cytochrome c oxidase of all species shows high activity and susceptibility to sulfide poisoning, with 50% inhibition at 30 to 500 nM in various tissues. The two marsh species are able to survive at sulfide concentrations already inhibitory to their cytochrome c oxidase and fatal to other species. All species detoxify sulfide by oxidizing it to thiosulfate. All have sulfide-oxidizing activity in the blood, spleen, kidney, liver and gills, which correlates significantly with heme content. Thiosulfate appears in the tissues of sulfide-exposed fish and builds up to high concentrations (up to 2 mM) with stronger and longer exposure. Unexposed fish contain little or no thiosulfate. Sulfide is barely detectable in the tissues, even in high-sulfide exposure tests. We suggest that fish blood, in having high sulfide-oxidizing activity and no cytochrome c oxidase, can act as a short-term first line of defense against sulfide, and thus minimize the amount that reaches the vital organs. The results of this study indicate that sulfide is a significant environmental factor influencing the ecological distribution of marine fishes.     

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.     

Genetic studies in marine fishes

Nine polymorphic loci were found among 42 presumptive protein-coding gene loci surveyed among 474 red drum (Sciaenops ocellatus) sampled in 1987 from 13 nearshore and 1 offshore localities from the Atlantic coast of the southeastern USA and the northern Gulf of Mexico. The mean number of alleles over the polymorphic loci was 3.8, and the average heterozygosity over all loci examined was estimated as 0.047. These data indicate that red drum have normal levels of genetic variability. Wright'sF1 _ST values (the standardized variance of allele frequencies between samples) over all polymorphic loci ranged from 0.009 to 0.027 (meanF1 _ST =0.019), and estimates of the effective number of migrants (N _e m) per generation using Wright's island model ranged from 9.0 to 27.5. High levels of gene flow among the red drum samples were also indicated by Slatkin's qualitative analysis using conditional average allele frequencies. Nei's estimates of genetic distance between pairs of samples ranged from 0.000 to 0.009, indicating a high degree of nuclear gene similarity among all samples. Highly significant heterogeneity in allele frequencies at the locus for adenosine deaminase was detected between red drum sampled from the Atlantic and those sampled from the Gulf and among red drum sampled from the Gulf.     

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.     

High pressure effects on marine invertebrates and fishes

A survey of literature and of new information from the author's laboratory is presented concerning the comparative pressure physiology of marine invertebrates and fishes. Short term experiments on littoral marine animals have revealed that the taxonomic groups exhibiting the greatest resistance to high pressures are those with the greatest vertical distributions in the deep sea, namely, echinoderms, molluscs, amphipods, isopods and polychaetes. Shallow water species which possess high thermal and osmotic resistance also show an exceptionally high degree of pressure resistance. The relative differences in genetic pressure resistance of lower marine invertebrates are the same in whole, intact animals and in isolated, surviving tissue pieces. Adaptation of nonregulating euryoecous invertebrates to higher temperatures, higher osmotic concentrations and higher calcium contents of the tissues results in increased pressure resistance. Under pressure, the optimum cellular pH shifts downward to a lower pH range.Lecture presented on October 23, 1967 at Duke University, Marine Laboratory, Beaufort (USA); on November 6, 1967 at the Instituto di Biologia Marinha of the University of São Paulo (Brasil); and on November 8, 1967 at the Institute of Marine Science of the University of Miami (USA).     

Chitinolytic enzymes in the digestive system of marine fishes

Chitinase, exo-N-acetyl--D-glycosaminidase (NAGase) and lysozyme activities were assayed in the digestive tract of 6 species of marine fishes: Myxine glutinosa (cyclostome), Chimaera monstrosa (holocephalan), Squalus acanthias, Etmopterus spinax, Raja radiata (elasmobranchs) and Coryphaenoides rupestris (teleost). Strong chitinase activity was found in the gastric mucosa of the elasmobranchs (S. acanthias, E. spinax and R. radiata) and the teleost (Coryphaenoides rupestris). A remarkably high chitinase activity occurred in the pancreas of the stomachless holocephalan fish Chimaera monstrosa. NAGase activity was strong in the digestive tract of all species. It could be concluded that marine fishes with diets consisting largely of chitinous invertebrates may display high chitinase and NAGase activities in their digestive system; however, only low chitinase activity was found in the intestine of the cyclostome Myxine glutinosa. Coryphaenoides rupestris gastric mucosa chitinase had one optimum activity at pH 1.25, whereas S. acanthias chitinase had two optima, at pH 1.6 and 3.6. The NAGase pH-activity curves from S. acanthias and R. radiata gastric mucosa displayed similar optima, at pH 4.5 and 4.25 respectively. Chimaera monstrosa pancreatic chitinase had a very strong optimum around pH 8 to 10, and one less strong at pH 3. These enzyme activities could not be separated by gel filtration or isoelectric focusing. The pI (isoelectric point) was approximately 4.9 for both enzymes. The molecular weight of the C. monstrosa pancreatic chitinase was estimated to be approximately 43 000. Lysozyme activity was absent or extremely weak in the material studied.     

In vivo marking of shallow-water and deep-sea amphipods by ingestion of bait mixed with fast green

Seven vital stains were mixed with fish muscle and fed to a sublittoral lysianassid (Orchomene sp. A collected in Scripps Canyon off La Jolla, California USA between August 1978 and August 1981) in the laboratory to test the utility of these dyes as feeding labels for scavenging amphipods. Fast-green FCF proved to be the most effective of the stains tested; >90% of starved amphipods fed fast-green-stained bait (Scomber japonicus muscle) for as little as 1 h exhibited a conspicuous green coloration along the digestive tract, which lasted an average of 35 d. The ability to label animals with such a single, short exposure interval makes this dye especially suitable for marking scavengers attracted to bait. Fast green efficiently stained this amphipod over a broad range of concentrations (1 to 8% by weight in water) and feeding regimes, and had no significant effects on survivorship or activity of laboratory-held organisms. Nile blue A also proved to be an acceptable feeding label for Orchomene sp. A for time scales of about 1 wk. Additional laboratory and field tests between August 1978 and August 1979 indicated that fast green is an effective feeding stain for 2 bathyal species (Orchomene sp. B and O. plebs from the Ross Sea, Antarctica) and 3 abyssal species (Eurythenes gryllus, O. gerulicorbis and Paralicella caperesca from the central North Pacific Ocean) of amphipods. Field labeling of amphipods at 5 800 m in the central North Pacific Ocean with fast green demonstrates that feeding stains may be used readily as in situ marking agents for population studies of scavengers in remote environments.     

Temporal resolution in the eyes of marine decapods from coastal and deep-sea habitats

 Temporal responses of eyes from four decapod species taken from sublittoral (Pandalus montagui Leach), coastal [Nephrops norvegicus (L.)] and deep-sea [Paromola cuvieri (Risso) and Chaceon (=Geryon) affinis A. Milne Edwards and Bouvier] habitats were examined. The electroretinogram responses to a range of sinusoidal intensity modulations between 0.5 and 40 Hz were recorded. Recordings were made from individuals adapted successively to two background light intensities. The sublittoral and coastal species showed faster responses when adapted to the higher light level and they also responded best to intermediate frequencies. When adapted to the lower light level, all species responded most strongly to low-frequency stimuli. Physiological and ecological reasons for the differences in responses are suggested. Received: 2 July 1999 / Accepted: 26 October 1999     

Species-specific patterns of hyperostosis in marine teleost fishes

The occurrence of swollen or hyperostotic bones in skeletal preparations, preserved museum material or whole fresh specimens of marine teleost fishes was identified in 92 species belonging to 22 families. Patterns of hyperostotic skeletal growth were typically consistent and often species-specific in all individuals larger than a certain size. The taxonomic distribution of hyperostosis in diverse phylogenetic groups suggests that it has arisen independently many times. Selected bones from two species of the family Carangidae, horse-eye jack Caranx latus Agassiz and crevalle jack Caranx hippos (Linnaeus), were examined in detail by light and electron microscopy. Nonhyperostotic bone contained osteoid-producing osteoblasts, resorbing osteoclasts, occasional osteocytes, and a rich vascular network, all characteristics of cellular bone. Thus, these fishes have a spatial juxtaposition of cellular and acellular bone tissues in adjacent and often serially homologous bone sites. The functional significance of hyperostosis is unknown, but it is a predictable manifestation of bone growth and development for the many taxa in which it occurs.     

In-situ studies on deep-sea amphipods and their intestinal microflora

Amphipods, trapped at depths of 1 410 to 5 330 m and incubated in situ in the presence of a radiolabeled protein as a food source, were fractionated to measure the distribution of label in the major biochemical constituents: low molecular pools, ethanol and base soluble proteins, lipids, polysaccharides and nucleic acids. The results suggest lipid energy storage and enhanced microbial growth within the amphipod guts as compared to growth on the uningested food material. The merits and limitations of this general approach are critically evaluated.     

Effects of UVB radiation in a microbenthic community of a marine shallow-water sandy sediment

The role of ambient and enhanced ultraviolet-B radiation (UVB; 280 to 315 nm) in a natural sand-associated microbenthic community was studied in a 3-week experiment by incubating intact sediment cores from a shallow bay in an outdoor flow-through system with 27 aquaria. After sampling of initial cores, the remaining cores (one per aquarium) were given one of three treatments: no, ambient, and moderately enhanced UVB, and sampled, nine at a time, after 5, 12, and 19 d. The response of the community was studied by analysing algal and meiofaunal composition and biomass, chlorophyll a content, composition of pigments and fatty acids, and content of UV-absorbing compounds (state variables), as well as carbon fixation and allocation, and bacterial productivity (rate variables). Among rate variables, significant effects of UVB-treatments were found for carbon fixation and allocation, while bacterial productivity was not affected. For state variables, a significant response was observed for the composition of microalgae and fatty acids, and for chlorophyll a content. The effect of treatments was mainly observed as differences in development with time (two-way analysis of variance, treatment × time interaction). Towards the end of the experiment, the no-UVB treatment most often differed from one or both of the two treatments with UVB exposure, the latter showing lower values. There were marked successional changes in the community, irrespective of treatment. The microalgal community changed from being dominated by coccoid cyanobacteria and epipsammic diatoms to a dominance of epipelic diatoms and filamentous cyanobacteria. The pattern of carbon allocation, as well as an increased C/N ratio of the sediment, suggested limitation of growth, perhaps by nutrients, at the end of the experiment. This may possibly have acted synergistically with UVB exposure to create the treatment effects. The new knowledge gained from our experiment is that ambient UVB can exert a stress on the function of sand-associated microbenthic communities in shallow waters and that this effect coincides with structural differences in the community. More experiments in natural or semi-natural systems are needed to allow better prediction of microbenthic community-level responses to UVB. Received: 11 November 1997 / Accepted: 12 June 1998     

Geographical gradients of marine herbivorous fishes: patterns and processes

We present new data and the first rigorous analysis of latitudinal and thermal gradients of diversity, density and biomass of marine herbivorous fishes and review proposed explanatory mechanisms. Consistently, negative relationships between latitude, and positive relationships between sea surface temperature (SST), and relative richness and relative abundance of herbivorous fishes were found worldwide. Significant differences in the strength of gradients of richness and abundance with latitude and SST between tropical and extratropical zones were found consistently across ocean basins. Standardized sampling along the western Atlantic also showed negative relationships between latitude and total density and biomass. The trends, however, are driven by different components of the fish assemblages (i.e., scarids in the Caribbean and acanthurids in Brazil). Patterns of abundance along thermal gradients, generally associated with extensive latitudinal gradients, also were found at the local scale. Feeding rate of the ocean surgeonfish Acanthurus bahianus decreases with temperature more rapidly than the mean metabolic rate of teleost fishes. This relationship suggests a temperature-related physiological constraint. From the new standardized and comparative data presented and the review of the explanatory hypotheses, we conclude that temperature-related feeding and digestive processes are most likely involved in the distribution patterns of herbivorous fishes. Electronic Supplementary Material Supplementary material is available for this article at     

Plasma nonesterified fatty acids of marine teleost and elasmobranch fishes

The plasma nonesterified fatty acids (NEFA) of five species of temperate zone marine teleost fishes (Northwestern Atlantic), one Arctic marine teleost (Eastern Canadian Arctic), and four species of marine elasmobranchs (Northwestern Atlantic) are reported. Four fatty acids, 16:0, 18:1n9, 20:5n3 and 22:6n3, comprised 70 to 83% of total NEFA in the plasma of all temperate teleost species examined. With the sole exception of 18:1, these differed from the predominant fatty acids, 14:1, 16:1, 18:1 and 20:5n3, in the Arctic species. The predominant fatty acids in elasmobranch NEFA were 16:0, 22:6n3 and 18:1n9 in all species but saturated fatty acids (14:0, 16:0 and 18:0) accounted for 40% of all NEFA in all elasmobranchs examined. Monoenes represented a greater, and polyenes a smaller, percentage of the fatty acids in the Arctic sculpin compared to the temperate sculpin. Fatty acids of the n3 series were lower in the plasma of the Arctic sculpin compared to the temperate sculpin. Comparisons with published values for freshwater fish using the same method indicate the n3:n6 ratio is higher in the marine teleost fishes. Ratios of n3:n6 fatty acids ranged from 1.80 to 7.94 for the elasmobranchs and were on average lower than those for the marine teleosts. Total levels of NEFA for the elasmobranchs were between 193 and 399 nmol ml^-1, lower than the values reported here for teleosts but within the range reported by others for some teleost fishes.     

Comparative study of metamorphosis in tropical reef fishes

This study explores the types of changes in pigmentation and morphology that occur immediately after settlement in 13 families of tropical reef fishes encompassing 34 species. The morphology of individual fishes was recorded daily from when they were first caught at night as they came into the vicinity of a reef to settle. Changes in pigmentation and morphology were species specific and often varied greatly among species within a family or genus. Pigmentation changes were typically rapid (<36 h) and dramatic. Morphological changes involved the elongation and regression of fin spines and changes in head shape and body depth. Eighteen percent of species experienced changes in snout shape and dorsal spine length of greater than 5%. Similarly, 15% experienced changes in pectoral fin length and head length of greater than 5%. Changes typically occurred gradually over 6 or more days, although in about 44% of the species the major change in one of the measured body dimensions occurred rapidly (within 36 h). Moderately strong positive relationships were found between both growth and developmental rates and the extent of metamorphosis in the damselfishes (Pomacentridae) (r=0.48 and 0.63, respectively). This suggests there may be a minimum level of development necessary to be a fully functional demersal juvenile. Although many of the changes that occur are subtle compared to the preceding development, these changes occur at an important ecological transition. Published online: 16 August 2002     

Temperate marine reserves enhance targeted but not untargeted fishes in multiple no-take MPAs.

Although many papers report the effects of no-take marine protected areas (MPAs or reserves), scientifically rigorous empirical studies are rare, particularly for temperate reef fishes. We evaluated the responses of fish populations to protection from fishing in reserves by comparing densities and sizes inside and outside of five no-take reserves in southern California, USA. Our results are robust because we compared responses across multiple rocky-reef reserves in two different years and controlled for possible site differences by (a) ensuring that habitat characteristics were the same inside and outside reserves, and (b) sampling species that are not targeted, which would not be expected to have a direct response to fishing. We compared fish density and size and calculated biomass and egg production across all five sites. Fishes targeted by recreational and/or commercial fisheries consistently exhibited increases in mean density (150%), size (30%), biomass (440%), and egg production (730%) inside reserves. Reserve effects were greatest for legal-sized targeted fishes: significantly greater densities were found exclusively inside reserves for targeted species (580%), the largest size classes existed only inside reserves, and mean biomass was 1000% higher. These responses were unlikely to have been caused by habitat differences because there were no significant differences in habitat characteristics between reserve and control locations. Densities of non-targeted species did not differ between reserve and non-reserve locations, further supporting the conclusions that differences in targeted species between reserve and control locations were due to harvesting rather than site-specific effects. Although MPAs cannot replace traditional fisheries management, the concentration of increased biomass and egg production is a unique MPA benefit that serves both reserves and fisheries. Scientifically rigorous studies that include multiple reserves, such as this study, are needed to inform management and policy decisions.