Ammonia excretion by zooplankton and its significance to primary productivity during summer

Excretion rates of ammonia have been determined for zooplankton off the coasts of Washington and Oregon (USA). Rates varied from 0.16 to 0.60 g-at NH ₄ ⁺ -N/mg dry weight/day for most planktonic animals, and from 0.02 to 0.06 for jellyfishes. Ammonia concentration in seawater was low in offshore regions. Ammonia released by zooplankton was studied in relation to primary productivity during summer. It was found that, in the Columbia River plume offshore, excreted ammonia contributed about 90% of the total nitrogen requirements of observed production rates. The ammonia-N contribution was 36% in oceanic waters, and was relatively unimportant in the inshore region. The significance of eddy diffusivity in offshore waters and upwelling in inshore waters is also discussed.Contribution No. 747 from the Department of Oceanography, University of Washington, Seattle, USA.     

Lipid composition of twenty-two species of Antarctic midwater zooplankton and fish

Total lipids, hydrocarbons, wax esters, triacylglycerols, and phospholipids were determined for 22 major biomass species of zooplankton and fish in an Antarctic mesopelagic community that were collected in 1982 and 1983. Lipid levels were similar to levels in more temperate mesopelagic species. Total lipid concentration was depth related, with all lipid-rich species being collected at depths greater than 230 m. Wax ester content in copepods (60 to 70% of the total lipid) was generally higher than in subtropical species. Lipids indicated three predator-prey relationships (Parandania boecki-Atolla wyvillei, Thysanoessa macrura-Calanoides acutus andEurythenes gryllus-Atolla wyvillei). These were confirmed by gut content analyses. The mesopelagic fishBathylagus antarcticus, Pleuragramma antarcticum, andProtomyctophum bolini stored most lipid intramuscularly, whereasElectrona antarctica andGymnoscopelus nicholsi contained extensive stores in subcutaneous lipid sacs. The intramuscular lipids inP. antarcticum and the subcutaneous lipid sacs ofE. antarctica were primarily wax esters, possibly used for increased buoyancy or long-term energy storage. Unlike the odd-carbon preference of aliphatic hydrocarbons which typifies terrestrial plants and temperate marine organisms, even-carbon chain-length paraffins predominate in 80% of the Antarctic species analyzed. Although the source of these even-carbon n-alkanes cannot be determined from our data, their dominance in the species analyzed suggests that an unusual biochemical pathway may be responsible for their synthesis in this ecosystem.     

Respiration and nitrogen excretion of zooplankton. IV. The influence of starvation on the metabolism and the biochemical composition of some species

Changes in the respiration, ammonia excretion and biochemical composition were studied for three species of starving zooplankton (Calanus finmarchicus, Sagitta elegans, and Acartia clausi). Over the period of starvation, the respiration rate of all three species followed the same pattern of an initial decrease followed by a more or less constant level. A similar pattern was observed for the ammonia excretion rate of S. elegans and A. clausi, whereas C. finmarchicus excretion appeared to oscillate between high and low levels of protein catabolism. Study of the biochemical changes showed that C. finmarchicus consumed primarily lipids, and at times proteins, to meet its energy requirement whereas S. elegans and A. clausi primarily used protein. Variations in the elemental composition as well as the O:N ratio confirmed that C. finmarchicus alternated between periods of protein-dominant catabolism and lipid-dominant catabolism during starvation. No similar change in catabolism was observed in the two other species. The results are discussed in terms of physiological mechanisms of resistance to starvation and were used to calculate the energy budget of S. elegans and C. finmarchicus during the period of total starvation. The significance of such budgets is discussed and some of the sources of error examined.Bedford Institute of Oceanography Contribution.     

Respiration and nitrogen excretion of zooplankton. II. Studies of the metabolic characteristics of starved animals

Respiration and nitrogen-excretion studies were carried out on several species of zooplankton (Meganyctiphanes norvegica, Phronima sedentaria, Acartia clausi and Sagitta setosa) under starvation. Although all the species were mainly ammonotelic, apparently a significant amount of organic nitrogen was excreted; the validity of the measurements and their significance are discussed. The effect of duration of starvation showed for M. norvegica and A. clausi two different patterns of behaviour, which were chiefly a function of the rate of biomass turnover of the species studied. The rates of metabolism, chemical composition, and reaction to starvation varied with season in M. norvegica. The physiological balance of the experimental animals was examined by calculating the protein carbon equivalent to respiratory and excretory catabolism, and by use of atomic O:N ratios. Starved individuals catabolized more protein carbon than can be accounted for by the amount of respiratory oxygen utilized. A hypothesis, which suggests that there are three levels of resistance to starvation, is proposed to explain this paradox, and its metabolic basis is discussed.     

Effects of prolonged starvation on O2 consumption,NH 4 + excretion,and chemical composition of the bathypelagic mysid Gnathophausia ingens

The large bathypelagic mysid Gnathophausia ingens was collected in January 1980 at 400 to 700 m depth from the San Clemente Basin off southern California. Instars 7-8 and Instars 10-12 were starved in the laboratory for up to 19 wk. Oxygen consumption and ammonia excretion rates, and water, protein, lipid, and ash contents were determined periodically during starvation. Protein and lipid were metabolized in approximately equal amounts by starved individuals after the initial weeks of food deprivation. Unidentified components (probably non-protein nitrogenous compounds) apparently were oxidized within the first 7 wk of starvation. Oxygen consumption and ammonia excretion by Instars 7-8 decreased steadily during 19 wk of starvation. In contrast, stable or increasing respiration and excretion rates were observed for fed mysids. The mean respiration rate of Instars 10-12 did not change significantly during 13 wk of starvation, although ammonia excretion rates decreased. Low metabolic rates and large lipid reserves probably help G. ingens to withstand long periods of starvation in the mesopelagic environment. Calculations based on the laboratory data demonstrate that small, infrequent meals could account for the rates of metabolism and growth observed for G. ingens in the field.     

Oxygen uptake,ammonia excretion and phosphate excretion by krill and other Antarctic zooplankton in relation to their body size and chemical composition

Oxygen uptake, ammonia excretion and phosphate excretion were measured in 14 Antarctic zooplankton species, including various size classes of krill (Euphausia superba), during a cruise to the Antarctic Ocean adjacent to Wilkes Land in the summer of 1980. Elemental composition (C, N and P) was also determined on the specimens used in these metabolic rate measurements. The values obtained for C, N and P were 4.7 to 47.5%, 1.2 to 12.5% and 0.09 to 1.23% of dry weight, respectively. Regression analyses of metabolic rates on different measures of body weight (fresh, dry, C, N and P) were made on krill, salps and other zooplankton as arbitrarily defined groups and also on the combined groups to determine the best measure of body weight for intra- and interspecific comparison of metabolic rates. The correlations were highly significant in all regressions, although no common measure of body weight provided the best correlation for the three groups of animals. Except for the regression of ammonia excretion on C and N weight, all other regressions of metabolic rates and body weights were significantly different within these three groups. In the combined group, oxygen uptake and ammonia excretion were better correlated to C and N weights than to dry and P weights. For phosphate excretion in the combined groups, dry weight gave the best correlation. Despite these results, the choice of a particular measure of body weight was shown to be important in a comparison of the rates between krill and salps because of their widely different chemical compositions. Our results of rate measurements are compared with those of previous workers for some Antarctic zooplankton, particularly krill. Some of the previous data are in good agreement with ours, while others are not. Possible contributing factors are considered in the latter case. The ratios between the rates (O:N, N:P and O:P) fell within the general ranges reported for zooplankton from different seas. The O:N ratio was consistently low (7.0 to 19.8, by atoms) in all species, suggesting the importance of protein in their metabolic substrates. Protein-oriented metabolism was also supported by the results of C and N analyses which indicated no large deposition of lipid in these animals. From the results of metabolic rate measurements and elemental analyses, daily losses in bodily C, N and P for Antarctic zooplankton in summer were estimated as 0.4 to 2.8%, 0.6 to 2.5% and 1.3 to 19.4%, respectively. These values are approximately one order of magnitude lower than those reported for subtropical and tropical zooplankton.     

In situ feeding rhythms of herbivorous copepods,and the effect of starvation

In situ diel variations in gut pigment contents of neritic (Acartia omorii andPseudocalanus minutus) and oceanic copepods (Calanus plumchrus andC. cristatus) were analyzed.A. omorii andP. minutus were sampled in Onagawa Bay on the east coast of Japan in May and August 1987, andC. plumchrus andC. cristatus were sampled in the Bering Sea in June 1986. Gut pigments were generally high at night, and bimodal feeding rhythms were observed in all species. The first peak of gut pigments occurred between sunset and midnight and was followed by a midnight decrease in gut pigment levels, resulting in eventual evacuation of the gut. The second peak was observed a few hours after sunrise. Incubation experiments indicated that ingestion rates of starved copepods were higher than those of acclimated copepods. This phenomenon was most notable at high food concentrations. Gut pigments of starved copepods rapidly increased after exposure to high concentrations of culturedThalassiosira decipiens. These findings suggest that in situ feeding behavior of herbivorous copepods includes periods of cessation or reduction in feeding during the night, and consequently, feeding activity is periodically enhanced with starvation. Starvation enhanced feeding behavior is most obvious in the large oceanic species,C. plumchrus andC. cristatus and is not distinct in small coastal species such asA. omorii.     

A comparison of carbon based ammonia excretion rates between gelatinous and non-gelatinous zooplankton: Implications and consequences

About 560 literature data on weight-specific ammonia excretion rates of gelatinous zooplankton (cnidarians, ctenophores and salps) and non-gelatinous zooplankton (mainly crustacea) were converted to carbon based units to enabel a better comparison between both groups. If carbon is used as body-mass unit ammonia excretion rates of gelatinous zooplankton are in the same range as values obtained for other zooplankton taxa, indicating a similar nitrogen output per unit of organic matter in both groups. These results suggest nutrient regeneration potential to be the same in gelatinous and non-gelatinous zooplankton, and that nutrient regeneration within the pelagic system depends more upon the carbon biomass ratio between gelatinous and other zooplankton than on physiological differences.     

Metabolic rates of midwater crustaceans as a function of depth of occurrence off the Hawaiian Islands: Food availability as a selective factor?

During July of 1983, 1986, and 1987, we measured rates of oxygen consumption of 234 individuals of 17 species of midwater crustaceans (orders Decapoda, Mysidacea, and Euphausiacea) off the Hawaiian islands at depths from the surface to greater than 1200 m. The routine metabolic rates declined with increasing depths of the species' occurrence to an extent greater than could be accounted for by depth-related changes in body size or water temperature. Most species appeared able to regulate their oxygen consumption down to the lowest oxygen partial pressures found in their depth range (20 mm Hg O₂), but did not regulate to such low oxygen partial pressures as did similar midwater crustaceans off California, where oxygen levels reach as low as 6 mm Hg. Metabolic rates of the shallower-living, but not the deepest-living Hawaiian crustaceans were significantly higher than those of Californian crustaceans. This is interpreted as indicating that the metabolic rates of midwater crustaceans are not adapted specifically to differing levels of primary production and that the decline with depth of metabolic rates in these species is not the result of food limitation at depth. The data are, however, consistent with the hypothesis that lower metabolic rates at depth are due to the relaxation of selection pressures relating to visual predation near the surface.     

The effect of laboratory conditions on the extrapolation of experimental measurements to the ecology of marine zooplankton. IV. Changes in respiration and excretion rates of boreal zooplankton species maintained under fed and starved conditions

Herbivorous zooplankton species (Calanus plumchrus, Paracalanus parvus and Euphausia pacifica) and carnivorous species (Parathemisto pacifica and Pleurobrachia pileus) collected from Saanich Inlet, British Columbia, Canada, were maintained in the laboratory under fed and starved conditions. Respiration rate and excretion rates of ammonia and inorganic phosphate were measured successively on the same batch populations of each species in different feeding conditions. Respiration rate remained at a constant level or increased during the feeding experiment but decreased progressively in starved individuals. Herbivorous, but not carnivorous, species showed a rapid decrease in both excretion rates for the first few days of an experiment irrespective of feeding conditions. However, the general level of excretion rates of fed specimens was higher than that of starved ones. The O:N, N:P and O:P ratios were calculated from respiration, ammonia excretion and phosphate excretion and discussed in relation to metabolic substrates of animals during the experiment. A marked difference was shown in the O:N ratio between fed hervivores (>16) and fed carnivores (7 to 19), suggesting highly protein-oriented metabolism in the latter. One unknown factor causing variation in excretion rates is speculated to be the physiological stress on animals during sampling from the field. It is suggested that the laboratory measurement of realistic excretion rates of zooplankton is difficult owing to their large fluctuations, but this is not the case with respiration rate.     

Metabolic rates of epipelagic marine zooplankton as a function of body mass and temperature

The metabolic rates (oxygen uptake, ammonia excretion, phosphate excretion) of epipelagic marine zooplankton have been expressed as a function of body mass (dry, carbon, nitrogen and phosphorus weights) and habitat temperature, using the multiple-regression method. Zooplankton data used for this analysis are from phylogenetically mixed groups (56 to 143 species, representing 7 to 8 phyla, body mass range: 6 orders of magnitude) from various latitudes (habitat temperature range:-1.4° to 30°C). The results revealed that 84 to 96% of variation in metabolic rates is due to body mass and habitat temperature. Among the various body-mass units, the best correlation was provided by carbon and nitrogen units for all three metabolic rates. Oxygen uptake, ammonia excretion and phosphate excretion are all similar in terms of body-mass effect, but differ in terms of temperature effect. With carbon or nitrogen body-mass units, calculated Q₁₀ values are 1.82 to 1.89 for oxygen uptake, 1.91 to 1.93 for ammonia excretion and 1.55 for phosphate excretion. The effects of body mass and habitat temperature on the metabolic quotients (O:N, N:P, O:P) are insignificant. The present results for oxygen-uptake rate vs body mass do not differ significantly from those reported for general poikilotherms by Hemmingsen and for crustaceans by Ivleva at a comparable temperature (20°C). The importance of a body-mass measure for meaningful comparison is suggested by the evaluation of the habitat-temperature effect between mixed taxonomic groups and selected ones. Considering the dominant effects of body mass and temperature on zooplankton metabolic rates, the latitudinal gradient of community metabolic rate for net zooplankton in the ocean is estimated, emphasizing the non-parallelism between community metabolic rates and the standing stock of net zooplankton.     

Chemical composition,metabolic rates and feeding behavior of the midwater ctenophore Bathocyroe fosteri

Individuals of the midwater ctenophore Bathocyroe fosteri (0.01 to 1.6 g dry weight, DW) were collected from Bahamian waters by the submersible Johnson-Sea-Link during May and September/October 1983 and October/November 1984 from 530 to 700 m depth. Metabolic rates were measured and showed oxygen consumption to be in the range of 0.01 to 0.18 mg O₂ g^-1 DW h^-1 at temperatures ranging from 9° to 12°C. Ammonium excretion (0.01 to 0.14 g-at N g^-1 DW h^-1) was typically low. Energy expenditures estimated from respiration data (ca. 7% body C d^-1) indicated that one to three midwater crustacean prey (ca. 150 g C d^-1) could provide the daily maintenance ration required by a 40 mm ctenophore. These metabolic characteristics complemented in situ observations of poor locomotor ability and passive feeding behavior.     

Dietary study of the midwater polychaete Poeobius meseres in Monterey Bay,California

This study presents the first quantification of the diet of a gelatinous midwater organism on a temporal basis. Using the Monterey Bay Aquarium Research Institute's remotely operated vehicle Ventana, regular collections of the polychaete Poeobius meseres (Heath, 1930) over a 1 yr period (October 1990 to November 1991) in Monterey Bay yielded intact organisms for the study of feeding behavior and quantitative analysis of stomach contents. In situ observations showed P. meseres feeding in two different ways: (1) by deployment of a mucus web in the water column that passively collects particles for consumption; and/or (2) by grasping detrital material in the water column with its ciliated tentacles. Stomach-content analyses showed that P. meseres is primarily coprophagic, its diet being dominated by fecal pellets from euphausiids and copepods. These fecal pellets appear to provide P. meseres with essentially all its carbon. Although fecal pellets were the most important food item volumetrically, P. meseres also consumed large numbers of diatoms and small numbers of dinoflagellates, chrysophytes, radiolarians, foraminiferans and eggs. The diet of P. meseres appears to reflect primary productivity in the surface waters, with different food items predominant in the diet at different times of the year. Pennate diatoms were most abundant in the diet during the fall, centric diatoms were most abundant during the sumnier, and fecal pellets during the winter. The composition of P. meseres diet suggests that this and other midwater gelatinous organisms have a significant role in the remineralization of particles as they sink from the surface to the deep sea.     

Ammonium excretion by gelationous zooplankton and their contribution to the ammonium requirements of microplankton in Chesapeake Bay

Ammonium excretion rates of recently collected specimens of gelatinous zooplankton, the scyphomedusan Chrysaora quinquecirrha DeSor and the etenophore Mnemiopsis leidyi A. Agassiz, were correlated with body mass and water temperature in measurements made from April to October 1989 and 1990. Rates ranged between 3.5 and 5.0 g atoms NH ₄ ⁺ -N (g dry wt)^-1h^-1 for C. quinquecirrha and 3.0 to 4.9 g atoms NH ₄ ⁺ -N (g dry wt)^-1h^-1 for M. leidyi. Excretion rate equations and in situ data on the size distributions and biomasses of gelatinous zooplankters and water temperature were used to estimate the contribution of ammonium by medusae and ctenophores to mesohaline Chesapeake Bay waters on several dates during April to October 1989 and 1990. We then compared the estimated contributions to direct measurements of ¹⁵NH ₄ ⁺ uptake by microplankton. The maximum estimated regeneration by gelatinous zooplankton was 5.8 g atoms NH ₄ ⁺ -N m^-3h^-1 at night in August 1990, when medusae biomass was greatest. This represents about 4% of the ammonium required by the microplankton. During the daytime on all dates, less than 1% of the ammonium required by microplanktion was supplied by gelatinous zooplankton. Therefore, gelatinous zooplankton appear to play a minor role in the ammonium cycle of Chesapeake Bay.     

Ammonia excretion of Artemia sp. (crustacea: Branchiopoda) under axenic conditions)

Ammonia excretion of the Utah strain of Artemia sp. grown in axenic culture media was followed throughout the different stages of larval development. The ammonia accumulated in the culture medium does not affect ammonia excretion rates under our laboratory conditions. Growth rate, density and starvation all affect ammonia excretion. Ammonia excretion is directly related to the numerical growth index and inversely related to Artemia sp. density. Starved adult Artemia sp. excrete considerably lower amounts of ammonia than brine shrimp grown in nutritive medium. In view of the difficulties often encountered in estimating the excretion rates of small crustaceans, our culture conditions would appear advantageous for further studies on the purine metabolism of Artemia sp.     

Metabolic properties of Northern krill, Meganyctiphanes norvegica, from different climatic zones. I. Respiration and excretion

Adaptive processes linked to overall metabolism were studied in terms of oxygen consumption and ammonia excretion in each of three self-contained krill populations along a climatic gradient. In the Danish Kattegat, krill were exposed to temperatures which ranged from 4°C to 16°C between seasons and a vertical temperature gradient of up to 10°C during summer. In the Scottish Clyde Sea, water temperatures varied less between seasons and the vertical temperature gradient in summer was only 3°C. Temperatures in the Ligurian Sea, off Nice, were relatively constant around 12-13°C throughout the year, with a thin surface layer (20-30 m) of warm water developing during summer. The trophic conditions were rich in the Kattegat and, particularly, in the Clyde, but comparatively poor in the Ligurian Sea. Oxygen consumption increased exponentially with increasing experimental temperature, which ranged from 4°C to 16°C. Overall respiration rates were between 19.9 and 89.9 µmol O₂ g^-1 dry wt h^-1. Krill from the Kattegat, the Clyde Sea, and the Ligurian Sea all exhibited approximately the same level of oxygen consumption (30-35 µmol O₂ g^-1 dry wt h^-1) when incubated at the ambient temperatures found in their respective environments (9°C, 5°C, and 12°C). This indicates that krill adjust their overall metabolic rates to the prevailing thermal conditions. The exception to this were the respiration rates of Ligurian krill from winter/spring, which were about twice as high as the rates from summer krill despite the fact that the thermal conditions were the same. This effect appears to result from enhanced somatic activity during a short period of increased food availability and reproduction. Accordingly, krill appears to be capable of adapting to both changing thermal and trophic conditions, especially when nutrition is a limiting factor in physiological processes.     

Behaviour of the institute of oceanographic science's rectangular midwater trawls: Theoretical aspects and experimental observations

The behaviour of two rectangular midwater trawls, the RMT 1+8 and the RMT 1+8M, is described. The RMT 1+8 consists of a pair of rectangular nets contained within the same frame-a small mouth area RMT 1 of mesh size 320 m and a larger RMT 8 of mesh size 4.5 mm. The RMT 1+8M is a multiple version of the RMT 1+8, combining three RMT 1s and three RMT 8s within the same frame. An expression is developed to describe the dependence of mouth angle on speed for the RMT 1+8 when towed horizontally. Theoretical estimates of the changes in mouth angle with speed agree well with experimental observations. Within normal towing speeds the RMT 1+8 is sensitive to changes in speed; this sensitivity is especially marked in the RMT 1. Between speeds of about 2.6 and 8.0 knots the RMT 8 does not alter its mouth angle with changes in speed; this behaviour is not shown by the RMT 1—at least within a practical speed range. The performance of the RMT 1+8M cannot be completely described by the theory developed for the RMT 1+8 and possible explanations for this are discussed. The multiple net is considerably less sensitive to changes in towing speed; all three nets of each type have similar mouth angles at a constant speed. Variations in warp load with speed for both trawls are described.     

Ammonia excretion by the benthic estuarine shrimp Crangon franciscorum (Crustacea: Crangonidae) in relation to diet

Ammonia excretion of individual Crangon franciscorum Stimpson was monitored in response to ingestion of single meals. The three experimental diets were tubificids, mysids and fish. Ammonia excretion was also monitored for individual shrimp which had been starved. The rate of ammonia excretion was higher for fed than for starved individuals in all cases. Ammonia excretion rates were higher for shrimp which were fed tubificids than those fed the other diets. The rate of excretion was influenced by both weight of the individual and the amount ingested of each diet. Ammonia excretion was influenced by dietary factors other than nitrogen content of the diet or the quantity ingested. The data suggest that field estimates of ammonia excretion based on the excretion rates of starved animals may be underestimates. The recent feeding history of an organism influences the rate of ammonia excretion as well as the relationship between the rate of excretion and weight.     

Metabolic activity and elemental composition of krill and other zooplankton from Prydz Bay,Antarctica, during early summer (November–December)

Oxygen uptake and ammonia excretion rates, and body carbon and nitrogen contents were measured in krill (Euphausia superba) and eight other zooplankton species collected during November–December 1982 in the Prydz Bay, Antarctica. From these data, metabolic O:N ratios (by atoms), body C:N ratios (by weight) and daily metabolic losses of body carbon and nitrogen were calculated as a basis from which to evaluate seasonal differences in metabolism and nutritional condition. Comparison of the present data with mid-summer (January) data revealed that early-summer E. superba were characterized by higher metabolic O:N ratios (58.7 to 103, compared with 15.9 to 17.5 for mid-summer individuals). Higher O:N ratios of early-summer E. superba resulted largely from reduced ammonia excretion rates and, to a lesser degree, from slightly increased oxygen uptake rates. Body C:N ratios of E. superba were low in early-summer (3.8 to 4.2) compared with mid-summer krill (4.1 to 4.7) due to lowered body-carbon contents in the former (42.6 to 43.6% compared with 43.2 to 47.5% dry weight of midsummer individuals); gravid females formed an exception, since no seasonal differences in body elemental composition were detected for these. No significant changes in water content (75.3 to 81.4% wet wt) and nitrogen content (9.9 to 11.1% dry wt) in E. superba were evident between the two seasons. Seasonal differences in metabolic rates and elemental composition were less pronounced in a salp (Salpa thompsoni), but a higher metabolic O:N ratio occurred in early-summer individuals. Interspecific comparison of the seven remaining zooplankton species studied with twelve species from mid-summer zooplankton investigated in an earlier study indicated that higher metabolic O:N ratios in early-summer are characteristic not only of herbivore/filter-feeders, but also of some carnivores/omnivores. No relationship between metabolic O:N ratios and body C:N ratios was apparent either intraspecifically or interspecifically, within or between early-summer and mid-summer seasons.