Effect of body mass, temperature and food deprivation on oxygen consumption rate of common cuttlefish Sepia officinalis

Grigoriou, Panagiotis; Richardson, Christopher A.

doi:10.1007/s00227-009-1272-4

Cited by 23 publications

(17 citation statements)

References 35 publications

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“…Following 3-5 days of fasting, at a temperature of 21°C, Ṁ O 2 was about one half that of the fed animals and remained the same during starvation. Consistent with this, in a similar experiment, Grigoriou and Richardson (11) found that, at a lower temperature of 15°C, metabolic rate began to differ from that of fed animals after ϳ10 days of food deprivation. The Ṁ NH 4 reported here are in the same range as that of the Chinese cuttlefish (Sepiella maindroni) (42); however, lower rates of Ṁ NH 4 for S. officinalis were reported earlier (2).…”

Section: Discussionmentioning

confidence: 53%

Metabolic rate and rates of protein turnover in food-deprived cuttlefish,Sepia officinalis(Linnaeus 1758)

Lamarre

MacCormack

Sykes

et al. 2016

American Journal of Physiology-Regulatory, Integrative and Comp

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To determine the metabolic response to food deprivation, cuttlefish (Sepia officinalis) juveniles were either fed, fasted (3 to 5 days food deprivation), or starved (12 days food deprivation). Fasting resulted in a decrease in triglyceride levels in the digestive gland, and after 12 days, these lipid reserves were essentially depleted. Oxygen consumption was decreased to 53% and NH4 excretion to 36% of the fed group following 3-5 days of food deprivation. Oxygen consumption remained low in the starved group, but NH4 excretion returned to the level recorded for fed animals during starvation. The fractional rate of protein synthesis of fasting animals decreased to 25% in both mantle and gill compared with fed animals and remained low in the mantle with the onset of starvation. In gill, however, protein synthesis rate increased to a level that was 45% of the fed group during starvation. In mantle, starvation led to an increase in cathepsin A-, B-, H-, and L-like enzyme activity and a 2.3-fold increase in polyubiquitin mRNA that suggested an increase in ubiquitin-proteasome activity. In gill, there was a transient increase in the polyubiquitin transcript levels in the transition from fed through fasted to the starved state and cathepsin A-, B-, H-, and L-like activity was lower in starved compared with fed animals. The response in gill appears more complex, as they better maintain rates of protein synthesis and show no evidence of enhanced protein breakdown through recognized catabolic processes.

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Section: Discussionmentioning

confidence: 53%

Metabolic rate and rates of protein turnover in food-deprived cuttlefish,Sepia officinalis(Linnaeus 1758)

Lamarre

MacCormack

Sykes

et al. 2016

American Journal of Physiology-Regulatory, Integrative and Comp

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“…In food-deprived juvenile S. officinalis, oxygen consumption was maintained for 6 days, but thereafter, it decreased to 35% of initial level by day 27. Following resumption of feeding, oxygen consumption immediately returned to control levels (15), revealing a maintenance of functional integrity of the oxygen delivery system. During the period of food deprivation associated with reduced oxygen consumption, we propose that there is a reduction in requirement for exposed lamellae.…”

Section: Perspectives and Significancementioning

confidence: 94%

“…In cuttlefish, Sepia officinalis, oxygen consumption is maintained for the first 6 days of starvation, and thus, rates of metabolic fuel delivery must remain constant (15). Collectively, the above implies that during periods of food deprivation, the limited lipid reserves are called upon first, in parallel with, then subsequently, followed by, an obligate dependence on the use of protein as a metabolic fuel.…”

mentioning

confidence: 99%

Mechanisms of protein degradation in mantle muscle and proposed gill remodeling in starvedSepia officinalis

Lamarre

Ditlecadet

McKenzie

et al. 2012

American Journal of Physiology-Regulatory, Integrative and Comp

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-Cephalopods have relatively high rates of protein synthesis compared to rates of protein degradation, along with minimal carbohydrate and lipid reserves. During food deprivation on board protein is catabolized as a metabolic fuel. The aim of the current study was to assess whether biochemical indices of protein synthesis and proteolytic mechanisms were altered in cuttlefish, Sepia officinalis, starved for 7 days. In mantle muscle, food deprivation is associated with a decrease in protein synthesis, as indicated by a decrease in the total RNA level and dephosphorylation of key signaling molecules, such as the eukaryote binding protein, 4E-BP1 (regulator of translation) and Akt. The ubiquitinationproteasome system (UPS) is activated as shown by an increase in the levels of proteasome ␤-subunit mRNA, polyubiquitinated protein, and polyubiquitin mRNA. As well, cathepsin activity levels are increased, suggesting increased proteolysis through the lysosomal pathway. Together, these mechanisms could supply amino acids as metabolic fuels. In gill, the situation is quite different. It appears that during the first stages of starvation, both protein synthesis and protein degradation are enhanced in gill. This is based upon increased phosphorylation of 4E-BP1 and enhanced levels of UPS indicators, especially 20S proteasome activity and polyubiquitin mRNA. It is proposed that an increased protein turnover is related to gill remodeling perhaps to retain essential hemolymph-borne compounds.cathepsin; cephalopod; metabolic enzymes; proteasome; polyubiquitin; RNA; starvation; triglyceride CEPHALOPODS TYPICALLY FEED upon protein-rich diets and are generally high in protein content with low reserves of lipid and carbohydrates. Most of the lipid is present in the digestive gland with very low lipid reserves in other tissues (33). Studies tracking the incorporation of radiolabeled phenylalanine into the protein pool show that in feeding cephalopods, protein accretion is favored by relatively low rates of protein degradation compared to rates of protein synthesis (6,18,27). In Southern dumpling squid (Euprymna tasmanica), whole body protein degradation increases in minimally fed animals (18). Furthermore in octopus, Octopus vulgaris, the oxygen consumption-nitrogen excretion ratio increased over the first 5 days of starvation to values that imply a mixed lipid and protein oxidation, and by day 8 the ratio decreased to a predominantly protein-based metabolism (5). In cuttlefish, Sepia officinalis, oxygen consumption is maintained for the first 6 days of starvation, and thus, rates of metabolic fuel delivery must remain constant (15). Collectively, the above implies that during periods of food deprivation, the limited lipid reserves are called upon first, in parallel with, then subsequently, followed by, an obligate dependence on the use of protein as a metabolic fuel. The objective of the current study was to assess whether biochemical indices of protein breakdown and to some extent protein synthesis in various tissues are altered du...

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“…Grigoriou and Richardson (2009) modeled the routine metabolism of laboratoryraised cuttlefish (Sepia officinalis); however, their data do not meet the selection criteria established in the present study, so no meaningful comparison can be conducted. As the only comparable interspecific Table 2 Regression statistics of pelagic cephalopods and fishes derived from stepwise (forward selection, P in = P out = 0.05) multiple regression analyses of routine respiration rates (R: μlO 2 individual −1 h −1 ) on body mass [BM, in terms of wet mass (WM), dry mass (DM), carbon (C) or nitrogen (N), all mg], habitat temperature (Temp, K) and habitat depth (Depth, m) [Model (1)], and plus 16 orders/families for cephalopods [Model (2)], or 15 orders for fishes [Model (3)].…”

Section: Effects Of Body Massmentioning

confidence: 96%

“…Compared with fishes, the respiration data available for pelagic cephalopods are modest (Seibel et al, 1997;Seibel, 2007;Grigoriou and Richardson, 2009;Hirst et al, 2014). Brey (2010) combined a large body of respiration data from diverse aquatic invertebrate taxa including 44 cephalopod species and established an empirical model to estimate the respiration rates as a function of the lifestyle features (i.e., feeding type, mobility type and vision type) and physiological states (fed or starved, and activity level) of these animals, along with the body mass, temperature and water depth as parameters.…”

Section: Introductionmentioning

confidence: 99%

Routine metabolic rates of pelagic marine fishes and cephalopods as a function of body mass, habitat temperature and habitat depth

Ikeda¹

2016

Journal of Experimental Marine Biology and Ecology

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Routine metabolic rates of pelagic marine fishes and cephalopods as a function of body mass, habitat temperature and habitat depth Tsutomu Ikeda 16-3-1001 Toyokawa-cho, Hakodate 040-0065, Japan a b s t r a c t Cephalopods and fishes are major components of marine micronekton and nekton, so an understanding of their physiology and roles in ocean biogeochemistry is important. I compiled the routine respiration rates (50 datasets on 41 cephalopod species; 102 datasets on 90 fish species) from various depth horizons (b1300 m) of the world's oceans and analyzed these rates as a function of body mass [wet mass (WM), dry mass (DM), carbon (C) or nitrogen (N)], habitat temperature and habitat depth using multiple regression. Stepwise-regression analyses revealed that body mass was the most important parameter, followed by habitat temperature and habitat depth, and these variables explained 89.7-93.8% and 94.7-95.8%, respectively, of the variance in the respiration data of fishes and cephalopods. The addition of a taxon category (order or family) as a fourth variable improved these correlations only slightly (95.6-95.7% and 95.7-96.2%, respectively). The resultant regression equation showed higher respiration rates in cephalopods than fishes relative to the DM, C or N body mass (by a factor 1.5-to 1.7-fold), but not to the WM body mass. The O:N ratios (respiration/ammonia excretion, by atoms) reported for 6 cephalopods (median: 13.2) and 35 fishes (24.2) suggested the predominance of protein as a metabolite in the former and carbohydrate or lipid in the latter. The present results are discussed in light of the methodological constraints and standing hypothesis for the relationship between the metabolic rate and temperature. The empirical models established in the present study can be used to assess the roles of cephalopods and fishes in C and N cycles in pelagic ecosystems based on the organisms' body mass spectra, ambient temperatures and depth distributions.

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Effect of body mass, temperature and food deprivation on oxygen consumption rate of common cuttlefish Sepia officinalis

Cited by 23 publications

References 35 publications

Metabolic rate and rates of protein turnover in food-deprived cuttlefish,Sepia officinalis(Linnaeus 1758)

Metabolic rate and rates of protein turnover in food-deprived cuttlefish,Sepia officinalis(Linnaeus 1758)

Mechanisms of protein degradation in mantle muscle and proposed gill remodeling in starvedSepia officinalis

Routine metabolic rates of pelagic marine fishes and cephalopods as a function of body mass, habitat temperature and habitat depth

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