Introduction
A good knowledge of the potential effects of water temperature on feeding and on-growing process is of primary importance to optimize the fish production. Temperature modulates ingestion, transit, digestion, assimilation, metabolism and ultimately feed utilization and growth rate. These two last parameters, together with the cost of feeds and energy, are necessary data for producers to make decisions. The production in indoor facilities with temperature control is depending on energy cost while in outdoor facilities (ponds and cages) it depends on environmental temperature. The effect of temperature is more noticeable in fast growing fish, as the greater amberjack (Seriola dumerili), a species of great interest for the aquaculture industry worldwide. Currently, its cultivation is expanding in the Mediterranean countries. Therefore, it constitutes a good model to study the consequences of an increased temperature. In this study, we examined the ingestion, digestive enzyme activities, metabolites in plasma and liver, antioxidant response in the liver and the integrity and electrogenic amino acid transport in the intestine, in greater amberjack juveniles growing at three different temperatures. The final aim was to elucidate the mechanisms behind feed utilization that justify the growth differences and to provide a useful informative basis to the productive sector.
Materials and methods
Greater amberjack juveniles (weight 23.35 ± 5.07 g; mean and SD) were randomly distributed in three independent RAS units set to 18, 22 and 26ºC of temperature, each one with three 900-L tanks. Juveniles were reared for 58 days under a photoperiod of 12h-light/12h-dark and fed until apparent satiation 3 times a day with a commercial diet (Skretting). Every two weeks, 5 fish per tank were sampled to check their body weight. At the end of the experiment, 16 fish per tank were sampled for assessing feeding and growth performance (weight gain, feed intake, feed conversion ratio) and analytical determinations. Luminal pH was measured in stomach and middle intestine. Activity of digestive proteases (trypsin, chymotrypsin, leu-aminopeptidase, pepsin) was analysed at the actual physiological temperature and pH. Oxidative stress biomarkers (protein carbonylation PC, catalase activity CAT, lipid peroxidation LPO, total antioxidant capacity TAC and mitochondrial reactive oxygen species mROS) were analysed in liver concomitantly with plasma cortisol; metabolites (triacylglycerol TAG, lactate, protein, glucose, glycogen, cholesterol) were also evaluated in plasma and liver. Intestinal integrity, permeability and electrogenic amino acid transport were assessed in using chambers. Differences were checked by ANOVA followed by Tukey’s test.
Results
Voluntary feed intake, final body weight and weight gain increased with the temperature increase from 18 to 26°C (p<0.05). Feed conversion ratio was higher at 18°C than at the other temperatures (p<0.05) (Table 1). Overall, the activities of trypsin and chymotrypsin were higher at 22°C than at 18ºC when analysed at their physiological temperature and pH (Fig. 1). Contrarily, pepsin was not detected at the actual physiological pH. In liver, TAG was higher at 18°C, whereas hepatic glucose and glycogen (Table 2), as well as plasma protein and cortisol levels were higher at 26°C. Oxidative stress parameters were higher at 18°C than at the other temperatures, excepting mROS that was similar among treatments. Epithelial electrophysiology showed that tissue resistance was temperature-dependent and the electrogenic amino acid transport was higher at 26°C than at the other temperatures.
Discussion
The tested temperatures are within the tolerance range described for this species. Ingestion clearly increased with the increase of temperature, but growth and FCR were similar at 22 and 26°C, although weight values were higher at 26°C. Interestingly the level of enzymatic activities was also similar at 22 and 26°C. In addition, the temperature increase modifies the intestinal epithelium selectivity and improves electrogenic amino acid transport from the lumen at least in the mid-intestine. At 26°C, fish are using primarily TAGs from liver for covering the energetic demand, while at 18°C switched to carbohydrates. The higher plasma protein level reflects a higher synthesis activity for growth. TAGs were less utilised at 18°C, with risk of liver steatosis, or even favouring damage by oxidative stress at the lowest temperature, despite activating antioxidant defences. From a practical view, 22 and 26°C appear as optimal temperatures for on-growing the species, although surely better growth would be obtained at 26°C in longer periods. At 18°C, the low ingestion and the damage derived from the oxidative stress impair the growth capacity.
Acknowledgements
Project THERMODIGEST, RTI2018-096134-B-I00 (MCIU-AEI, Spain + FEDER).