Metabolic suppression in thecosomatous pteropods as an effect of low temperature and hypoxia in the eastern tropical North Pacific

Author Posting. © The Author(s), 2011. This is the author's version of the work. It is posted here by permission of Springer for personal use, not for redistribution. The definitive version was published in Marine Biology 159 (2012): 1955-1967, doi:10.1007/s00227-012-1982-x.Many pteropod species in the eastern tropical north Pacific Ocean migrate vertically each day, transporting organic matter and respiratory carbon below the thermocline. These migrations take species into cold (15-10ºC) hypoxic water (< 20 µmol O2 kg-1) at depth. We measured the vertical distribution, oxygen consumption and ammonia excretion for seven species of pteropod, some of which migrate and some which remain in oxygenated surface waters throughout the day. Within the upper 200 meters of the water column, changes in water temperature result in a ~60-75% reduction in respiration for most species. All three species tested under hypoxic conditions responded to low O2 with an additional ~35-50% reduction in respiratory rate. Combined, low temperature and hypoxia suppress the metabolic rate of pteropods by ~80-90%. These results shed light on the ways in which expanding regions of hypoxia and surface ocean warming may impact pelagic ecology.This work was funded by National Science Foundation grants to K. Wishner and B. Seibel (OCE – 0526502 and OCE – 0851043) and to K. Daly (OCE – 0526545), the University of Rhode Island, and the Rhode Island Experimental Program to Stimulate Competitive Research Fellowship program.2013-06-3

Physiological and behavioral aspects of Calanus euxinus females (Copepoda : Calanoida) during vertical migration across temperature and oxygen gradients

In the Black Sea, during summer stratification, Calanus euxinus (Hulsemann) undertakes diel vertical migrations with an amplitude of about 117 m from oxygenated, warm (18 degreesC) surface layers to hypoxic (similar to0.8 mg O-2 l(-1)) zones with lower temperature (7.9 degreesC). When such changes in temperature and oxygen concentration are reproduced in the laboratory, total metabolism, basal metabolism and scope of activity of copepods decrease 7.2, 7.8 and 6.7 times, respectively, while the frequency of locomotory acts and mechanical power decline 3.4- and 9.5-fold, respectively. These changes allowed the copepods to conserve a significant portion of food consumed near the surface for transformation to lipid reset-yes. Diel respiratory oxygen consumption of migrating individuals, calculated so as to include actual duration of residence in layers with different temperature and oxygen concentrations, is estimated at 17.87 mug O-2 ind(-1) The net energy cost of vertical migration made up only 11.6% of the total. Copepods expend 78.6% of diel energy losses during approximately 10 h in the surface layers, while about 5.4% is required during about 9 h at depth Hypoxia is shown to have a significant metabolic advantage during diel vertical migrations of C. euxinus in the Black Sea

Development and lipid storage in Calanus euxinus from the Black and Marmara seas: Variabilities due to habitat conditions

Oil sac volume, gonad size and moulting patterns were investigated in the copepod Calanus euxinus inhabiting deep and shallow zones of the Black Sea and penetrating into the Marmara Sea. In summer the C. euxinus population in deep layers of the Black Sea was dominated by pre-diapause and diapausing postmoult copepodite stage V (CV) with small sexually undifferentiated gonads and mean lipid content of 14.1 +/- 6.0% of body volume. The lipid content of deep-living females was 7.2 +/- 4.2% of body volume. At the same time, intermoult and premoult CV with enlarged gonads and low lipid content (7.7 +/- 5.1% of body volume) and females with oil sac volume of 1.4 +/- 1.0% were found at shallow stations. Premoult CV with oil volume of 0.6 0.8% and mature females with little visual evidence of substantial lipid storage dominated in the Marmara Sea. The differences in moulting patterns and oil sac volumes of C. euxinus from deep zones and shallow regions suggest that vertical migrations to the oxygen minimum zone (OMZ) are necessary for formation of large lipid reserves providing high reproductive potential of this species. On the basis of an energy balance model it was shown that under low phytoplankton concentration of about 30 mu g C 1(-1) preadults and adults migrating to the OMZ could accumulate lipids (up to 5% of body energy content daily), in contrast to copepods constrained to shallow oxic water columns of the Black Sea and from the Marmara Sea. (c) 2005 Elsevier B.V. All rights reserved

Development and lipid storage in Calanus euxinus from the Black and Marmara seas: Variabilities due to habitat conditions

Oil sac volume, gonad size and moulting patterns were investigated in the copepod Calanus euxinus inhabiting deep and shallow zones of the Black Sea and penetrating into the Marmara Sea. In summer the C. euxinus population in deep layers of the Black Sea was dominated by pre-diapause and diapausing postmoult copepodite stage V (CV) with small sexually undifferentiated gonads and mean lipid content of 14.1 +/- 6.0% of body volume. The lipid content of deep-living females was 7.2 +/- 4.2% of body volume. At the same time, intermoult and premoult CV with enlarged gonads and low lipid content (7.7 +/- 5.1% of body volume) and females with oil sac volume of 1.4 +/- 1.0% were found at shallow stations. Premoult CV with oil volume of 0.6 0.8% and mature females with little visual evidence of substantial lipid storage dominated in the Marmara Sea. The differences in moulting patterns and oil sac volumes of C. euxinus from deep zones and shallow regions suggest that vertical migrations to the oxygen minimum zone (OMZ) are necessary for formation of large lipid reserves providing high reproductive potential of this species. On the basis of an energy balance model it was shown that under low phytoplankton concentration of about 30 mu g C 1(-1) preadults and adults migrating to the OMZ could accumulate lipids (up to 5% of body energy content daily), in contrast to copepods constrained to shallow oxic water columns of the Black Sea and from the Marmara Sea

Development and lipid storage in Calanus euxinus from the Black and Marmara seas: Variabilities due to habitat conditions

Oil sac volume, gonad size and moulting patterns were investigated in the copepod Calanus euxinus inhabiting deep and shallow zones of the Black Sea and penetrating into the Marmara Sea. In summer the C. euxinus population in deep layers of the Black Sea was dominated by pre-diapause and diapausing postmoult copepodite stage V (CV) with small sexually undifferentiated gonads and mean lipid content of 14.1 +/- 6.0% of body volume. The lipid content of deep-living females was 7.2 +/- 4.2% of body volume. At the same time, intermoult and premoult CV with enlarged gonads and low lipid content (7.7 +/- 5.1% of body volume) and females with oil sac volume of 1.4 +/- 1.0% were found at shallow stations. Premoult CV with oil volume of 0.6 0.8% and mature females with little visual evidence of substantial lipid storage dominated in the Marmara Sea. The differences in moulting patterns and oil sac volumes of C. euxinus from deep zones and shallow regions suggest that vertical migrations to the oxygen minimum zone (OMZ) are necessary for formation of large lipid reserves providing high reproductive potential of this species. On the basis of an energy balance model it was shown that under low phytoplankton concentration of about 30 mu g C 1(-1) preadults and adults migrating to the OMZ could accumulate lipids (up to 5% of body energy content daily), in contrast to copepods constrained to shallow oxic water columns of the Black Sea and from the Marmara Sea. (c) 2005 Elsevier B.V. All rights reserved

Respiration rates of Beroe ovata in the Black Sea

Metabolic rates of the ctenophore Beroe ovata within the length range from 0.4 mm (newly hatched larvae) to 60 mm were investigated. At 20degreesC the respiration rates (Q, mug O-2 ind.(-1) h(-1)) of individuals with wet weights (W, mg) less than or greater than 100 mg changed according to the equations Q=0.093W(0.62) and Q=0.016W(0.99), respectively. The weight-specific respiration rate of the juvenile ctenophores with wet body weights of 0.021-100 mg diminished approximately 20-fold (from 0.35 to 0.017 mug O-2 mg(-1) h(-1), respectively), but did not change within the range from 100 to 30,000 mg. The difference in the slope of the regression lines seems to be attributable to the ontogenetic changes in B. ovata metabolism. For the tested temperature range of 10-28degreesC, the mean Q(10) coefficient was equal to 2.17+/-0.5. The basal metabolism of B. ovata narcotised by chloral hydrate was 4.5+/-0.9 times lower than total metabolism. Such a metabolic range is considered to be characteristic of aquatic invertebrates with high levels of locomotory activity

Effect of starvation on the biochemical compositions and respiration rates of ctenophores Mnemiopsis leidyi and Beroe ovata in the Black Sea

The proximate biochemical composition and metabolic rates of ctenophores Mnemiopsis leidyi and Beroe ovata from the Black Sea were examined with respect to starvation conditions. Although organic matter content in B. ovata was two times higher than that of M. leidyi (2.51 +/- 0.53 and 1.4 +/- 0.17 mg g(-1) of wet weight, respectively), these species did not significantly differ in their biochemical composition. In both species protein formed about 80% of the total organic matter, lipids amounted to about 10%. Carbohydrate and amino acids measured separately made up less than 6.5% of the total organic matter. Under experimental starvation (18 days at 16-18 degrees C for B. ovata and 8 days at 12.4 degrees C for M. leidyi), wet weights of both ctenophore species were reduced by 9.4% and 9.3% d(-1), respectively. The rate of organic matter decrease was nearly two times lower than that of wet weight being on average 5.9% d(-1) in M. leidyi and 5.5% d(-1) in B. ovata. There was no trend in percentage of the four major biochemical categories with starvation time. The glycogen content in polysaccharides reached maximum values in freshly collected ctenophores (76.0 +/- 7.9% in B. ovata, and 86.6% in M. leidyi), but it was reduced substantially (34.4 +/- 2.7% in B. ovata and 18.3-28.8% in M. leidyi) with starvation. Monosaccharide content, expressed as a percentage of total carbohydrate, decreased from 39.9% to 13.5% in B. ovata, and from 45.8% to 14.3-23.2% in M. leidyi. The relationship between respiration rate (R) and wet weight (W) of individuals during the starvation can be expressed by power function R = R-1 W-k (r(2)=0.85-0.94; P<0.001) for both ctenophore species. On average, k values were 0.95 and 0.83 in B. ovata and in M. leidyi, respectively. By the end of the starvation, metabolic rate per unit wet weight decreased by 33% in B. ovata and 46% in M. leidyi. Organic matter utilization was almost totally explained by respiration of ctenophores in the experiments and exceeded metabolic requirements of studied species by 11% and 15%, correspondingly. As compared with Mnemiopsis, Beroe has better tolerance to starvation which explains to some extent the success of the species survival during prolonged periods of food shortage in the Black Sea conditions

Population dynamics, ingestion, growth and reproduction rates of the invader Beroe ovata and its impact on plankton community in Sevastopol Bay, the Black Sea

The impact of the introduced ctenophore Beroe ovata on its prey Mnemiopsis leidyi, another invader ctenophore voraciously feeding on mesozooplankton, and consequently on the mesozooplankton community, was evaluated by undertaking both laboratory and field studies in the northern Black Sea. Ingestion and growth rates as well as the gross growth efficiency of B. ovata were estimated from laboratory experiments. The daily ration of ctenophores was related to food abundance within a wide range of prey concentration and never reached saturation. Beroe ovata required high food rations (not less than 20% of body weight per day) for growth. The abundances, biomasses and population structures of these two introduced ctenophore species were also monitored, along with mesozooplankton, in inshore waters of the northern Black Sea (i.e. Sevastopol Bay and adjacent regions) over a period of 3 years (1999-2001) which is after B. ovata's arrival. The annual dynamics of the M. leidyi population were similar for the last 3 years: very low abundances and biomass values were observed during most of the year (unlike the previous years), with a sudden increase in summer-early autumn, but only for about a 2 month period. The B. ovata bloom during the peak M. leidyi biomass resulted in the M. leidyi biomass falling sharply to extremely low values. The predatory impact of M. leidyi on prey zooplanton was found to be reduced during the period of study compared with before

Nutritional condition of female Calanus euxinus from cyclonic and anticyclonic regions of the Black Sea

The content and composition of lipids in Calanus euxinus females were studied in cyclonic and anticyclonic regions in the southern Black Sea during the period of persistent density stratification (September 1996). The lipid content of C, euxinus from cyclonic regions was greater than of individuals from anticyclonic regions (average 101.9 and 58.8 mu g ind.(-1), respectively). Total Lipid content (mainly wax esters, 70 to 72%, and triacylglycerols, 8 to 13%) of female C. euxinus was correlated with chlorophyll a (chl a) (mean integrated concentration) (r = 0.92, p < 0.005). The high correlation with chi a was shown also for wax ester content. used as a long-term index of food supply (r = 0.89, p < 0.05). The correlation between triacylglycerol content (a short-term index) and chi a was not significant (r = 0.66, p < 0.2). In cyclonic regions the mean integrated chi a concentration (0.38 mg m(-3)) (as an indicator of phytoplankton food biomass) was 1.7-fold higher than in anticyclonic areas. The same trend occurred for mean integrated concentrations of nitrate and phosphate (0.996 and 0.299 mu M in cyclonic and 0.438 and 0.061 mu M in anticyclonic regions. respectively) in the chi a containing layer. Thus, conditions for total primary productivity in cyclonic regions were more favorable than in anticyclonic ones. This was consistent with lipid levels in female C, euxinus