Protein synthesis in crustaceans: a review focused on feeding and nutrition

This review aimed to place crustacean research on in vivo protein synthesis into a broader context, assess its potential for providing further insights into crustacean nutrition and physiology, and recommend future directions relevant to crustacean aquaculture. In crustaceans the flooding dose measurement of protein synthesis is the only method that has been used, it is relatively complex, time consuming and uses radioactive labels. Protein synthesis provides a subtle approach to assessing imbalances and deficiencies in dietary amino acid and energy. In addition, the calculation of protein synthesis retention efficiency (SRE) is recommended in order to understand and optimize parameters such as feeding regime and diet composition. For prawns, SRE was highest at optimum dietary protein content and quality. Similarly the most efficient feeding regimes in juvenile lobsters were demonstrated by the highest efficiency of retaining synthesized protein. Understanding how various abiotic and biotic factors influence protein synthesis has great potential for improving different aspects of crustacean aquaculture but very few studies have done this; better knowledge of how abiotic and biotic factors affect crustacean protein synthesis will contribute to optimising growth of crustaceans in culture.     

Some effects of temperature on respiration in decapodan crustaceans

Temperature variation effects respiration rate, acid-base balance and transport of respiratory gases by the haemolymph in crustaceans. Their responses to hypoxia and salinity variation are temperature dependent, as in the threshold for the onset of facultative air-breathing.     

The effects of temperature on walking and righting in temperate and Antarctic crustaceans

Antarctic marine invertebrates live in a cold, thermally stable environment and cannot tolerate large changes in body temperature (i.e. they are stenothermal). Their temperate relatives, by contrast, are eurythermal, living in warmer and thermally more variable environments. Have these different environments influenced how specific behaviours are affected by changes of temperature? This question was addressed in two temperate crustaceans, the decapod Carcinus maenas and isopod Ligia oceanica, and two Antarctic crustaceans, the isopod Glyptonotus antarcticus and amphipod Paraceradocus gibber. The thermal dependence of walking speed was analysed by contrasting the slopes of the linear part of each species’ behavioural curve. Over the temperature ranges analysed, the temperature sensitivity of walking speed in the stenotherms was 13–23% that of the eurytherms when measured in body lengths s^?1. There was a linear relationship between walking speed and temperature up to +4.5°C in the Antarctic species G. antarcticus and P. gibber. Elevating temperature by up to 3.5°C above the maximum temperature experienced in the Antarctic (+1°C), does not lead to an acute breakdown of motor coordination. We describe for the first time the righting behaviour of G. antarcticus. The mean time-to-right tended to a minimum on warming from ?2 to+5°C, but this trend was not statistically significant. Our results suggest that the physiological adaptations which permit continued activity at low Antarctic temperatures have resulted in a lower thermal dependence of activity in Antarctic species, compared to related temperate species.     

Effects of temperature on the specific dynamic action of the southern catfish, Silurus meridionalis

Specific dynamic action (SDA), the energy expended on all physiological processes that is associated with meal digestion and assimilation, is strongly affected by temperature. We assessed the effects of temperature on the postprandial metabolic response and calculated SDA of the southern catfish, Silurus meridionalis. The fish was fed with experimental diets at a meal size of 4% body mass, and by using an 8-chamber, continuous-flow respirometer the oxygen consumption rate was determined at a 2 h interval until the postprandial oxygen consumption rate returning to the preprandial level, at four different temperatures. The energy expended on SDA (SDA(E)) were 2.71, 3.07, 3.16, and 3.62 kJ, the SDA(coefficients) (energy expended on SDA quantified as a percentage of the digestible energy content of the meal) were 7.70, 9.44, 10.36, and 11.12%, and the peak metabolic rates (R(peak)) of SDA were 3.48, 4.31, 5.96, and 7.30 mg O2 h(-1), at 17.5, 22.5, 27.5, and 32.5 degrees C respectively. The relationships between those parameters and temperature were: SDA(E)=1.74+0.0559T (n=26, r(2)=0.676), SDA(coefficient)=4.10+0.223T (n=26, r(2)=0.726), and R(peak)=-1.34+0.264T (n=26, r(2)=0.896). The SDA durations showed a slow-fast-slow tendency of decrease with increasing temperature, and were 88.00, 85.71, 67.71, and 66.50 h at 17.5, 22.5, 27.5 and 32.5 degrees C respectively. Two separate peaks appeared during the SDA response at 17.5 degrees C, and it might be due to a rapid startup of the mechanical process with a lag of the biochemical process, which suggested that the peaks of "mechanical component" and "biochemical component" of SDA might be separated when temperature was low enough.     

The cost of a hot meal: facultative specific dynamic action may ensure temperature homeostasis in post-ingestive endotherms.

1. Resting metabolic rate was determined in Adelie penguins (Pygoscelis adeliae) that had been fed warm and cold ingesta. 2. Post-ingestion metabolic rate was found to be related to food temperature rather than to specific dynamic action. 3. Calorimetric calculations indicate that up to 13% of Adelie penguin daily energy expenditure may be used heating ingested food to body temperature. 4. Heating food costs are predicted to be higher in endotherms living in cold regions and in species with low assimilation efficiencies, but may be minimized by appropriate foraging behaviour.     

Ultraviolet and temperature effects on planktonic rotifers and crustaceans in northern temperate lakes

1. Anthropogenic stressors such as climate change, ozone depletion and acidification may act in concert to alter ultraviolet (UV) light and temperature regimes in freshwater ecosystems. These physical and chemical changes will inevitably affect zooplankton community dynamics, but little is known about their relative effects on different species in natural communities. During spring, species that migrate to surface waters to take advantage of warmer temperatures may be especially vulnerable as UV levels can be high. 2. The objective of this study was to investigate the in situ effects of UV and temperature on a natural assemblage of planktonic rotifers and crustaceans during the spring. We performed in situ exposure experiments in two lakes with different surface temperatures. 3. Exposure to UV had a significant effect on the abundance and/or reproduction of four rotifers: Gastropus spp., Kellicottia bostonensis, Kellicottia longispina, Keratella spp.; two cladocerans: Holopedium gibberum, Daphnia catawba, and one copepod: Leptodiaptomus minutus. Incubation under cooler temperatures had a negative effect on K. longispina and H. gibberum. Temperature and UV had a significant interactive effect on abundance and/or reproduction of L. minutus and Ploesoma truncatum. Our results indicate that changes in underwater UV and temperature can significantly influence the composition of the zooplankton community and ultimately food web dynamics.     

Effects of temperature on the specific dynamic action of the southern catfish, Silurus meridionalis.

Specific dynamic action (SDA), the energy expended on all physiological processes that is associated with meal digestion and assimilation, is strongly affected by temperature. We assessed the effects of temperature on the postprandial metabolic response and calculated SDA of the southern catfish, Silurus meridionalis. The fish was fed with experimental diets at a meal size of 4% body mass, and by using an 8-chamber, continuous-flow respirometer the oxygen consumption rate was determined at a 2 h interval until the postprandial oxygen consumption rate returning to the preprandial level, at four different temperatures. The energy expended on SDA (SDA(E)) were 2.71, 3.07, 3.16, and 3.62 kJ, the SDA(coefficients) (energy expended on SDA quantified as a percentage of the digestible energy content of the meal) were 7.70, 9.44, 10.36, and 11.12%, and the peak metabolic rates (R(peak)) of SDA were 3.48, 4.31, 5.96, and 7.30 mg O2 h(-1), at 17.5, 22.5, 27.5, and 32.5 degrees C respectively. The relationships between those parameters and temperature were: SDA(E)=1.74+0.0559T (n=26, r(2)=0.676), SDA(coefficient)=4.10+0.223T (n=26, r(2)=0.726), and R(peak)=-1.34+0.264T (n=26, r(2)=0.896). The SDA durations showed a slow-fast-slow tendency of decrease with increasing temperature, and were 88.00, 85.71, 67.71, and 66.50 h at 17.5, 22.5, 27.5 and 32.5 degrees C respectively. Two separate peaks appeared during the SDA response at 17.5 degrees C, and it might be due to a rapid startup of the mechanical process with a lag of the biochemical process, which suggested that the peaks of "mechanical component" and "biochemical component" of SDA might be separated when temperature was low enough.     

Effects of meal size,meal type,and body temperature on the specific dynamic action of anurans

Specific dynamic action (SDA), the increase in metabolism stemming from meal digestion and assimilation, varies as a function of meal size, meal type, and body temperature. To test predictions of these three determinants of SDA, we quantified and compared the SDA responses of nine species of anurans, Bombina orientalis, Bufo cognatus, Ceratophrys ornata, Dyscophus antongilli, Hyla cinerea, Kassina maculata, Kassina senegalensis, Pyxicephalus adspersus, and Rana catesbeiana subjected to meal size, meal type, and body temperature treatments. Over a three to seven-fold increase in meal size, anurans experienced predicted increases in postprandial rates of oxygen consumption the duration of elevated and SDA. Meal type had a significant influence on the SDA response, as the digestion and assimilation of hard-bodied, chitinous crickets, mealworms, and superworms required 76% more energy than the digestion and assimilation of soft-bodied earthworms, waxworms, and neonate rodents. Body temperature largely effected the shape of the postprandial metabolic profile; peak increased and the duration of the response decreased with an increase in body temperature. Variation in body temperature did not significantly alter SDA for four species, whereas both H. cinerea and R. catesbeiana experienced significant increases in SDA with body temperature. For 13 or 15 species of anurans ranging in mass from 2.4 to 270 g, SMR, postprandial peak and SDA scaled with body mass (log–log) with mass exponents of 0.79, 0.93, and 1.05, respectively.     

The relationship between specific dynamic action and otolith growth in pike

The hypothesis was tested that the daily increment width (IW) of the otolith comprises two components, one that correlates with basal metabolic rate (as has been demonstrated previously) and the other that correlates with apparent specific dynamic action ( R _sda)(the post‐prandial elevation in metabolism). Simultaneous measurements of IW and metabolic rate before and after a meal were collected from individual pike Esox lucius . After feeding, IW and metabolic rate increased above basal levels for 5–6 days. There was no correlation between daily IW and R _sda, reflecting within‐individual difference in the shapes of the post‐prandial responses of the two variables. There was a significant relationship between the total changes of IW and metabolic rate integrated following meals. The magnitude of the post‐prandial response as a proportion of the basal level was larger for metabolic rate than IW, mirroring the previously reported responses of these variables to acute temperature change. This study suggests that analysis of IW has the potential to provide a historic record of energy intake but only when integrated over a period equivalent to the digestion time. Consideration of energy budget theory indicates that IW is unlikely to provide a robust record of short‐term somatic growth if activity metabolism is significant and variable.     

Relationship between specific dynamic action and protein deposition in calanoid copepods

The link between specific dynamic action (SDA) and protein deposition was investigated in copepodites stage V of two calanoid copepod species, the neritic Acartia tonsa and the oceanic Calanus finmarchicus. This was done by measuring respiration before, during, and after a specific feeding period and measuring the incorporation of carbon into proteins. These were also measured on individuals incubated with cycloheximide, an antibiotic that inhibits protein synthesis. The cycloheximide treatment significantly diminished the magnitude of SDA in both A. tonsa and C. finmarchicus, and inhibited carbon incorporation into protein in both species. This provides evidence that the rate at which protein deposition takes place greatly affects the magnitude of SDA. The specific respiration rates of both starving and feeding copepods were generally higher in A. tonsa than in C. finmarchicus. This influenced SDA, the magnitude of SDA normalised to an 8 h feeding period being threefold higher in A. tonsa (78.7+/-25.7 nlO(2) μgC(-1)) than in C. finmarchicus (27.5+/-11.6 nlO(2) μgC(-1)). This difference may arise due to differences in energy allocation in the organisms of the copepodite V stage of the two species. In this stage C. finmarchicus deposits large quantities of storage lipids, predominately wax esters, whereas A. tonsa deposits proteins during somatic growth.     

Towards an explanation of specific dynamic action (SDA)

Of the hypotheses proposed to explain specific dynamic action (SDA), it is suggested that the 'protein synthesis/growth' theory offers the best basis for further research. In the light of this, the relationships between rates of protein synthesis and metabolic rates are examined. Both of which are depressed with increasing periods of starvation and there appears to be a link between rates of protein synthesis and thyroid activity. SDA may represent a short-term increase in rates of protein synthesis and turnover following feeding and the process is possibly regulated via plasma levels of thyroid hormones.     

Effects of ration size and hypoxia on specific dynamic action in the cod

We present the first data on the effect of hypoxia on the specific dynamic action (SDA) in a teleost fish. Juvenile cod (Gadus morhua) were fed meals of 2.5% and 5% of their wet body mass (BM) in normoxia (19.8 kPa Po(2)) and 5% BM in hypoxia (6.3 kPa Po(2)). Reduced O(2) availability depressed the postprandial peaks of oxygen consumption, and to compensate for this, the total SDA duration lasted 212.0+/-20 h in hypoxia, compared with 95.1+/-25 h in normoxia. The percentage of energy associated with the meal digestion and assimilation (SDA coefficient) was equivalent between the different feeding rations but higher for fish exposed to hypoxia. Comparing peak oxygen consumption during the SDA course with maximum metabolic rates showed that food rations of 2.5% and 5% BM reduced the scope for activity by 40% and 55%, while ingestion of 5% BM in hypoxia occupied 69% of the aerobic scope, leaving little energy for other activities.     

The energetics of Calanus euxinus: locomotion, filtration of food and specific dynamic action

The effect of locomotor activity on respiration rate was studiedin the food-deprived copepod Calanus euxinus tethered to a forcesensor. The power generated by mouth appendages during cruisinglocomotion, with a frequency of 40 Hz, accounted for 0.026 and0.0031 W for metabolic and mechanical processes, respectively.To overcome total hydrodynamic drag during foraging with a meanswimming speed of 3.2 cm s^–1, the copepods need 0.4 x10^–3 W, equating to 1.3% of total metabolism. The lossesof mechanical energy for body propulsion amounted to 1.3 x 10^–3W, whilst the cost of feeding current generation run up to 1.8x 10^–3 W, or 58% of the total. Changing of locomotor activityand respiration rate during feeding was examined separatelyin tethered and free-swimming copepods. At algal concentrationof 300 µg C L^–1, the magnitude of specific dynamicaction (SDA) averaged 1.2 ± 0.44 nL O₂ µg C^–1h^–1 in copepodites V and females, with similar movingactivity before and during feeding. The contribution of SDAinto total metabolism varied from 23 to 85% in C. euxinus withlow activity level and constituted only 10% in active animals.In starved copepods, with low locomotor activity, feeding eventsstimulated the increase in frequency and total duration of locomotionwhich resulted in elevated energy expenditure enhancing the‘apparent SDA’.